Global traffic and disease vector dispersalAndrew J. Tatem*†‡, Simon I. Hay*†, and David J. Rogers*

*Department of Zoology, University of Oxford, South Parks Road, Oxford OX1 3PS, United Kingdom; and †Malaria Public Health and Epidemiology Group,Centre for Geographic Medicine, Kenya Medical Research Institute, P.O. Box 43640, 00100 Nairobi GPO, Kenya

Edited by Kenneth W. Wachter, University of California, Berkeley, CA, and approved February 21, 2006 (received for review September 27, 2005)

The expansion of global air travel and seaborne trade overcomesgeographic barriers to insect disease vectors, enabling them tomove great distances in short periods of time. Here we apply acoupled human–environment framework to describe the historicalspread of Aedes albopictus, a competent mosquito vector of 22arboviruses in the laboratory. We contrast this dispersal with therelatively unchanged distribution of Anopheles gambiae and ex-amine possible future movements of this malaria vector. We use acomprehensive database of international ship and aircraft trafficmovements, combined with climatic information, to remap theglobal transportation network in terms of disease vector suitabilityand accessibility. The expansion of the range of Ae. albopictusproved to be surprisingly predictable using this combination ofclimate and traffic data. Traffic volumes were more than twice ashigh on shipping routes running from the historical distribution ofAe. albopictus to ports where it has established in comparison withroutes to climatically similar ports where it has yet to invade. Incontrast, An. gambiae has rarely spread from Africa, which wesuggest is partly due to the low volume of sea traffic from thecontinent and, until very recently, a European destination for mostflights.

Aedes albopictus � air travel � Anopheles gambiae � biological invasion �shipping

Throughout history the opening of travel and trade routesbetween countries has been accompanied by the spread of

microbes and their vectors (1). Significant events include the14th- to 17th-century plague pandemics, the 19th-century chol-era epidemics, and the escape of Aedes aegypti from West Africa,facilitating yellow fever epidemics in North American port citiesin the 19th and early 20th centuries (2). The most devastatingdisease vector introduction in recent history was that of Anoph-eles gambiae (3, 4), the most important malaria vector in Africa,to northeastern Brazil in 1930. Although malaria was alreadyendemic in the area, the greater vectorial capacity of thismosquito species, relative to local species, sparked Plasmodiumfalciparum malaria epidemics costing 16,000 lives (5) beforeeradication of An. gambiae by an effective, yet costly, controlprogram (6).

During the last 50 years air travel passenger numbers havegrown by nearly 9% per annum (7); shipping traffic has increasedby �27% since 1993 (8). This growth is associated with risingnumbers of cases of biological invasion. Gradual mixing of theworld’s biota represents a global problem, with consequencesranging from native species’ decline to threats to human health(9). Biological invasion is a multistep process involving initialdispersal, establishment, and spread (10, 11). Invasion researchhas increased considerably over the past 15 years, yet the initialdispersal phase, on which the other stages rely, remains the leaststudied (9). Recent biological invasions have involved bothdisease vectors (12) and the expansion or reemergence ofvector-borne diseases (13).

Modern transport facilitates the movement of disease vectorsfarther and faster than ever before. Aircraft have been provencapable of transporting disease vectors through experiments(14), the phenomenon of airport malaria (15), and incomingflight surveys (16). Air travel is also suspected to be directlyresponsible for the dispersal and consequent establishment of

exotic mosquitoes on many Pacific islands, including Hawaii (12,17). Modern container ships are known to have introducednumerous alien mosquito species, including the Asian tigermosquito, Aedes albopictus (18), to new areas (12). Ae. albopictusis of medical and public health concern because it has beenshown in the laboratory to be a highly efficient vector of 22arboviruses, including dengue, yellow, and West Nile feverviruses (19, 20). In the wild, however, its efficiency as a vectorappears to be generally low (19, 20), although it has beenimplicated in recent dengue fever outbreaks in the absence of theprincipal vector, Ae. aegypti (20, 21). From its Old Worlddistribution reported in 1930 (Fig. 1), Ae. albopictus expanded itsrange first to the Pacific Islands (20) and then, within the last 20years, to other countries in both the Old World and the NewWorld (Fig. 1) (20, 22), principally through ship-borne trans-portation of eggs and larvae in tires (23).

Although distance may no longer represent a significantbarrier to vector movement, climate at the point of entry stillpresents a fundamental constraint to establishment, becausesmall invertebrates are very sensitive to the weather. Here wecombine data on global air and sea traffic volumes with climaticdata to examine the effects of these constraints on global diseasevector dispersal and establishment. By remapping the globaltransport network in terms of climatic similarity, we examineboth how predictable was the spread of Ae. albopictus and whatmight be the potential for future dispersal of both Ae. albopictusand An. gambiae.

ResultsFig. 2 displays climatic dendrograms for the global shippingnetwork (Fig. 2 A) and the global air travel network (Fig. 2B).The dendrograms are climate-based phenetic trees that repre-sent the global transport network remapped in terms of suit-ability for each disease vector. The cutoff level on the seaportsdendrogram that included 90% of ports within the Old Worlddistribution of Ae. albopictus encompassed a single branch. Thisbranch consisted of two major subbranches reflecting the trop-ical and temperate Ae. albopictus races (24), with the remaining10% of ports displaying quite distinct environments (Mormugao,New-Mangalore, and Kuching). Ninety percent of airportswithin the preexpansion distribution of Ae. albopictus wereencompassed in a single branch of the airport dendrogram, buttemperate and tropical races were again distinguishable withinthis branch.

From �25,000 possible sea routes and �6,000 air routes, Table1 shows the top 10 shipping and air travel routes identified ashaving the highest relative invasion risk (defined in Materials andMethods) for Ae. albopictus and whether or not this species hasbeen recorded at the arrival port. We attempted to quantify therelative importance of sea traffic volume and local climate in theestablishment of Ae. albopictus by examining all 68 ports withinthe invasion risk dendrogram branches. Some (n � 21) ports

Conflict of interest statement: No conflicts declared.

This paper was submitted directly (Track II) to the PNAS office.

Freely available online through the PNAS open access option.

‡To whom correspondence should be addressed. E-mail: andy.tatem@zoo.ox.ac.uk.

© 2006 by The National Academy of Sciences of the USA

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were within the original range of Ae. albopictus, but, of the other47, to date just over half are in regions colonized or wherebreeding populations have been found. Within this group of 47ports, the average climatic distances of the invaded (n � 24) andnoninvaded (n � 23) ports were identical, but average sea trafficvolumes were significantly (2.43 times) greater in the formerthan the latter (41.84 ship visits per annum per route for invadedports and 17.24 for noninvaded ones; t � 2.343, P � 0.0024).

Fig. 3 shows the 10 sea traffic routes identified with thestrongest risk factors for importation and establishment of eachof four principal members of the An. gambiae complex. Theresults of the air traffic analysis for the African mosquitoes arenot displayed here because the current European bias in flightroutes from Africa and the climatic differences between the twocontinents mean that few risk routes were identified.

DiscussionThere is excellent correspondence between the predicted top 10 riskroutes in Table 1 and the global spread or interception of Ae.albopictus. Three of the top 10 shipping routes run from Japan tothe southeast United States, where some of the earliest breedingpopulations of Ae. albopictus were found and identified as origi-nating from Japan (12). Genoa, the destination of two more routesfrom Japan, was one of the earliest European cities to report Ae.albopictus, which was established there by 1990 (25); the vector hassince become the most important local nuisance mosquito (20). Ofthe remaining routes in Table 1, interceptions of Ae. albopictus intire shipments from Japan to Australasia have been made in bothBrisbane (26) and Auckland (27), but the species appears not tohave established, probably an endorsement of the strict localinspection and fumigation policies (12). There is no documentedevidence of invasion of Fraser, Canada, by Ae. albopictus. Given theclimatic similarity of ports in Japan and Fraser and the level ofshipping traffic between the two, Fraser should be considered athigh risk, especially because Ae. albopictus has already been inter-cepted at nearby Seattle (28).

Traffic volumes within the global transport network have beenproposed as important in determining biological invasion suc-cess (29–31). The role of shipping depends on a range of factors,such as ship type and destination port (32). Although it has beensuggested that invasion pressure (the number of arriving prop-agules) is not a simple function of total ship arrivals, the present

analysis suggests that the combination of traffic volumes andclimatic suitability can explain a great deal of the global spreadof Ae. albopictus and that, when the climatic suitabilities of sitesare similar, shipping volume alone appears to determine invasionprobability.

Although air travel is not implicated in the spread of Ae.albopictus, 6 of the 10 highest-risk air transport routes (Table 1)link the original range of Ae. albopictus with Honolulu in Hawaii,where this species has become established (33), whereas theremaining destinations have all reported interceptions of thismosquito. Recent work suggests that air travel was indeed themost likely route of invasion for Ae. albopictus to Hawaii (17).Details on Hawaiian ports were not available in the sea trafficdatabase.

Although the efficiency of Ae. albopictus as a disease vectorremains unclear, the An. gambiae complex of African mosquitoesare proven efficient vectors of P. falciparum malaria. Theirestablishment outside Africa, which has been the subject ofrecent speculation (34), could have devastating consequences(6). The results in Fig. 2 show that An. gambiae sensu stricto andAnopheles melas, from the hotter, wetter parts of tropical Westand Central Africa, are more likely to thrive in climaticallyequivalent zones in Southeast Asia and Central�South America.In contrast, Anopheles arabiensis prefers drier climates, whichmatch those of the Middle East and Canary Islands, whereasAnopheles quadriannulatus prefers relatively cooler habitats insouthern Africa that are matched most closely by those else-where in South Africa, Mediterranean Europe, and Japan. Ineach case, the combination of local climate and volume of seatraffic determines the areas at greatest risk of invasion. Unlikethe Ae. albopictus risk routes, however, there is no evidence ofAn. gambiae invasion at any of these destinations to date. Thisabsence of invasion may be partly explained by the relatively lowsea traffic volumes originating from most African ports, whichare only 1�10th (An. melas and An. quadriannulatus inhabitedareas), 1�20th (An. arabiensis), and 1�30th (An. gambiae sensustricto) of the average volumes of traffic on the Ae. albopictusroutes in Table 1. These figures appear to reinforce the conclu-sion about the importance of traffic volume, although An.gambiae sensu lato may also be less prone to move than Ae.albopictus because it is less well adapted to anthropogenic

Fig. 1. Old World distribution of Ae. albopictus (red), countries reporting established breeding populations of Ae. albopictus in the last 30 years (orange), andcountries reporting Ae. albopictus interception at ports (yellow).

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breeding sites, such as tires (3, 4), and is less frequently found inurban areas (35).

In contrast to the sea routes, which originate in Africa andhave distant destinations in ecologically equivalent environ-ments, the air travel network from the African continent isprimarily to European destinations, outside of the climaticsuitability limits of An. gambiae s.l. The air transport destinationsmost at risk are, therefore, generally to be found within thecontinent itself or are very close to it. Thus, we identify existingpotential risks of air transfer of An. arabiensis to the Middle Eastand of An. quadriannulatus from Mozambique to SouthernEurope (Lisbon). The air transport climate dendrogram alsoidentifies climatic similarities to Africa in both South Americaand Southeast Asia, but these were not linked by any directf lights in the database used for this analysis. Recently, however,long-haul flights from Africa direct to Washington, DC; Beijing;Hong Kong; and Bangkok, Thailand, have been opened, con-

siderably increasing the risk of introducing malaria vectors fromAfrica.

There are currently no confirmed examples of vector estab-lishment arising from air travel (12), although there is circum-stantial evidence that this has occurred (12, 16, 36). This modeof transport, however, may be more important in delivering thedisease, rather than the vector, via infected human passengers(37, 38). Furthermore, the continuing rise in imported andairport malaria cases (39, 40), the spread of insecticide resistancein mosquitoes, and antimalarial drug-resistant malaria parasites(41, 42) are all reflections of an expanding global air transportnetwork, increased travel to malarious countries (43), anddeclining aircraft disinsection (16).

Successful biological invaders can be difficult to predictgiven the lack of evidence of a universal trait related toinvasion (44). The identification here, however, of the princi-pal routes of movement of Ae. albopictus from thousands of

Fig. 2. Climatic similarity dendrogram for the major seaports of the world (A Inset) and the major international airports of the world (B Inset), with a sampleof the branches relating to the spread of Ae. allopictus in close-up on each.

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possible alternatives is evidence that seaports and airportswithin the global transport network at greatest risk of futurespread of disease vectors can be highlighted through a com-bination of climate and traffic data. Such an approach can,therefore, be used to prioritize monitoring, inspection, andquarantine efforts. Future challenges involve incorporatingmore sophisticated climatic data and extra variables, as well asinformation on shipping and aircraft specifics, intraspeciescompetition, vector infection rates, human populations at risk,seasonality, breeding site availability, disinsection, and landtransport routes.

It is being increasingly recognized that future progress in thefields of emerging diseases and ecology requires a holisticperspective incorporating multiple-scale social, physical, andbiological dimensions (45). The study of disease vector dis-persal must encompass scales from the study of microbialpathogens and arthropod vectors to the global scale of eco-logical processes affected by humans. Continuing globalizationwill increase the relative risks of establishment of a range ofvectors, as will many aspects of global climate change (46).There is no room for complacency because, whereas quaran-tine services must succeed every time, disease vectors needsucceed only once to establish new bridgeheads from which toinvade new regions or continents.

Materials and MethodsTransport Matrices and Climatic Signatures. Estimates of theamount of traffic among the 243 most visited internationalseaports in 2000 (30) yielded measures of traffic volumes on atotal of 29,403 routes. Data on total air passenger numbersmoving between the world’s 278 principal international air-ports in 2000 were also obtained (OAG Worldwide). Air andsea transport matrices were produced, with each cell contain-ing the number of air passenger or ship movements betweeneach port. The locations of the seaports and airports weresuperimposed onto nine gridded global climate surfaces (47)representing means, maximums, and minimums of tempera-ture, rainfall, and humidity, each rescaled to the same range of

values. Each 10 � 10 (�18 � 18 km at the equator) grid squarecovering the seaport�airport location was identified. To ensurea representative climate measure, up to eight land pixelssurrounding each seaport�airport grid square were identifiedwhere possible. Any seaports�airports located on islands toosmall to be represented by the climate surfaces were eliminatedfrom the analysis, reducing the sample size to 241 seaportsand 259 airports. The selected grid square data from thenine climate surfaces thus formed the climatic ‘‘signature’’ ofeach port.

Hierarchical Clustering and Climatic Envelopes. The distance inclimatic space between each seaport�airport signature andevery other seaport�airport signature was calculated to pro-duce separate seaport and airport ‘‘climatic dissimilarity’’matrices. Euclidean distance measures were used becausethere were generally too few pixels for any more sophisticatedmeasures of environmental distance. In the few cases wherethey could be applied, more complex statistical measures ofdistance did not affect the results. To remap the globaltransportation network in terms of disease vector accessibility,each climatic dissimilarity matrix was subjected to hierarchicalclustering by using an agglomerative algorithm (PHYLIP V3.63,University of Washington). The clustering results were thentranslated into dendrograms based on centroid linkage tomap the world’s seaport and airport connections by climaticsimilarity.

To examine how predictable was the spread of Ae. albopictus,each seaport and airport location was overlaid on a map of themosquito’s Old World range (Fig. 1) (20, 24, 48) and classifiedas either inside or outside the historical distribution. Thoseseaports�airports within the distribution were located on therelevant dendrogram. The dendrogram branch that encom-passed at least 90% of the ports was designated as defining thelimits of Ae. albopictus ’ ‘‘climatic suitability envelope.’’ In doingthis, we allowed for the fact that Ae. albopictus has bothtemperate (diapausing) and tropical (nondiapausing) races with

Table 1. Ae. albopictus shipping and air travel risk routes

Rank From ToAe. albopictus

found?Ae. albopictusestablished?

Shipping1 Chiba, Japan New Orleans Y Y2 Chiba, Japan Genoa, Italy Y Y3 Chiba, Japan Fraser, Canada N ?4 Chiba, Japan Brisbane, Australia Y ?5 Chiba, Japan Auckland Y ?6 Chiba, Japan South Louisiana Y Y7 Yokohama, Japan Fraser, Canada N ?8 Kobe, Japan Fraser, Canada N ?9 Chiba, Japan Miami Y Y

10 Yokohama, Japan Genoa, Italy Y YAir

1 Tokyo Narita, Japan Honolulu Y Y2 Osaka Kansai, Japan Honolulu Y Y3 Nagoya, Japan Honolulu Y Y4 Tokyo Narita, Japan Seattle Y ?5 Tokyo Narita, Japan Brisbane, Australia Y ?6 Fukuoka, Japan Honolulu Y Y7 Seoul, South Korea Honolulu Y Y8 Tokyo Hareda, Japan Honolulu Y Y9 Taipei Chang, Taiwan Seattle Y ?

10 Tokyo Narita, Japan Portland, OR Y ?

Air results are exclusive of short-haul routes to Hong Kong; Sapporo, Japan; and Pyongyang, North Korea.

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distinct environmental requirements and different original geo-graphical distributions (24).

Assuming the availability of suitable habitats and breedingsites and no interspecific competition, the chance of a vectorbecoming established on introduction is considered highest ifthe climate at any new (previously uninvaded) site is similar tothat at sites within its historical distribution (49). Those

seaports�airports not within the historical distribution of Ae.albopictus, but linked via a dendrogram branch within theenvironmental envelope, were therefore considered to besimilar enough climatically for there to be a risk of vectorestablishment.

Where sufficient seaport and airport data existed within thepredicted range of each mosquito (50), the above procedure was

Fig. 3. The 10 sea traffic routes identified with the strongest risk factors for importation and establishment of each of four principal members of the An.gambiae complex. (A) An. gambiae sensu stricto (s.s.). (B) An. arabiensis. (C) An. quadriannulatus. (D) An. melas.

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repeated for the malaria vectors, An. gambiae sensu stricto, An.arabiensis, An. quadriannulatus, and An. melas.

Risk Matrices. The risks of invasion were quantified as a functionof climatic similarity and traffic volume between the origin anddestination seaport�airport by rescaling independently theclimatic dissimilarity and sea�air traffic matrices to a rangebetween 0 (climates of the seaports�airports in question verydifferent; no traffic between them) and 1.0 (climates identicalor traffic high). The product of these rescaled measures was

taken to represent relative invasion risk for the sites on thedendrograms.

We are indebted to Briony Boon, John Drake, Carlos Guerra, BethPurse, Sarah Randolph, Paul Reiter, Dave Smith, and Robert Snow forcomments on earlier drafts of the manuscript, as well as two anonymousreviewers for valuable input. We are especially grateful to John Drakefor the generous supply of the sea traffic estimates. A.J.T. and S.I.H. arefunded by Research Career Development Fellowship 069045 (to S.I.H.)from the Wellcome Trust.

1. McNeill, W. H. (1976) Plagues and People (Anchor, New York).2. Tatem, A. J., Rogers, D. J. & Hay, S. I. (2006) Adv. Parasitol. 62, 297–347.3. Gillies, M. T. & De Meillon, B. (1968) The Anopheline of Africa South of the

Sahara (South African Inst. for Medical Research, Johannesburg).4. Gillies, M. T. & Coetzee, M. (1987) A Supplement to the Anopheline of Africa

South of the Sahara (South African Inst. for Medical Research, Johannesburg).5. Soper, F. L. & Wilson, D. B. (1943) Anopheles gambiae in Brazil: 1930 to 1940

(Rockefeller Foundation, New York).6. Killeen, G. F., Fillinger, U., Kiche, I., Gouagna, L. C. & Knols, B. G. J. (2002)

Lancet Infect. Dis. 2, 618–627.7. Upham, P., Thomas, C., Gillingwater, D. & Raper, D. (2003) J. Air Transport

Manage. 9, 145–151.8. Zachcial, M. & Heideloff, C. (2003) ISL Shipping Statistics Yearbook 2003 (Inst.

of Shipping Economics and Logistics, Bremen, Germany).9. Puth, L. M. & Post, D. M. (2005) Ecol. Lett. 8, 715–721.

10. Elton, C. S. (1958) The Ecology of Invasions by Animals and Plants (Methuen,London).

11. Shigesada, N. & Kawasaki, K. (1997) Biological Invasions: Theory and Practice(Oxford Univ. Press, Oxford).

12. Lounibos, L. P. (2002) Annu. Rev. Entomol. 47, 233–266.13. Gratz, N. G. (1999) Annu. Rev. Entomol. 44, 51–75.14. Russell, R. C. (1989) Travel Med. Int. 7, 26–31.15. Isaacson, M. (1989) Bull. W. H. O. 67, 737–743.16. Gratz, N. G., Steffen, R. & Cocksedge, W. (2000) Bull. W. H. O. 78, 995–1004.17. Kilpatrick, A. M., Gluzberg, Y., Burgett, J. & Daszak, P. (2004) Ecohealth 1,

205–209.18. Hawley, W. A. (1988) J. Am. Mosquito Control Assoc. 4, 1–40.19. Gubler, D. J. (2003) Lancet 3, 751–752.20. Gratz, N. G. (2004) Med. Vet. Entomol. 18, 215–227.21. Effler, P. V., Pang, L., Kitsutani, P., Vorndam, V., Nakata, M., Ayers, T., Elm,

J., Tom, T., Reiter, P., Rigau-Perez, J. G., et al. (2005) Emerging Infect. Dis. 11,742–749.

22. Moore, C. G. & Mitchell, C. J. (1997) Emerging Inf. Dis. 3, 329–334.23. Reiter, P. (1998) J. Am. Mosquito Control Assoc. 14, 83–94.24. Hawley, W. A., Reiter, P., Copeland, S., Pumpuni, C. B. & Craig, G. B. (1987)

Science 236, 1114–1115.25. Romi, R., Di Luca, M. & Majori, G. (1999) J. Am. Mosquito Control Assoc. 15,

425–427.

26. Kay, B. H., Ives, W. A., Whelan, P. I., Barker-Hudson, P., Fanning, I. D. &Marks, E. N. (1990) Med. J. Aust. 153, 31–34.

27. Laird, M., Calder, L., Thornton, R. C., Syme, R., Holder, P. W. & Mogi, M.(1994) J. Am. Mosquito Control Assoc. 10, 14–23.

28. Centers for Disease Control. (1986) Morbid. Mortal. Wkly. Rep. 35, 649–651.29. Levine, J. M. & D’Antonio, C. M. (2003) Conserv. Biol. 17, 322–326.30. Drake, J. M. & Lodge, D. M. (2004) Proc. R. Soc. London Ser. B 271, 575–580.31. Lockwood, J. L., Cassey, P. & Blackburn, T. (2005) Trends Ecol. Evol. 20,

223–228.32. Verling, E., Ruiz, G. M., Smith, L. D., Galil, B., Miller, A. W. & Murphy, K. R.

(2005) Proc. R. Soc. London Ser. B 272, 1249–1256.33. Mitchell, C. J. (1995) J. Vector Ecol. 20, 44–58.34. Powell, J. R. & Coluzzi, M. (July 21, 2004) in International Herald Tribune,

Opinion.35. Hay, S. I., Guerra, C. A., Tatem, A. J., Atkinson, P. M. & Snow, R. W. (2005)

Nat. Rev. Microbiol. 3, 81–90.36. Mangili, A. & Gendreau, M. A. (2005) Lancet 365, 989–996.37. Wenzel, R. P. (1996) N. Engl. J. Med. 334, 981–982.38. Hufnagel, L., Brockmann, D. & Geisel, T. (2004) Proc. Natl. Acad. Sci. USA

101, 15124–15129.39. Muentener, P., Schlagenhauf, P. & Steffen, R. (1999) Bull. W. H. O. 77,

560–566.40. Toovey, S. & Jamieson, A. (2003) Travel Med. Infect. Dis. 1, 167–175.41. Roper, C., Pearce, R., Nair, S., Sharp, B., Nosten, F. & Anderson, T. (2004)

Science 305, 1124.42. Okeke, I. (2004) Science 306, 2039–2040.43. Loutan, L. (2003) Int. J. Antimicrob. Agents 21, 158–163.44. Gewin, V. (2005) PLoS Biol. 3, 2066–2071.45. Wilcox, B. A. & Colwell, R. R. (2005) Ecohealth 2, 244–257.46. Rogers, D. J., Randolph, S. E., Lindsay, S. & Thomas, C. (2001) in Health

Effects of Climate Change in the U.K. (U.K. Dept. of Health, London).47. New, M., Lister, D., Hulme, M. & Makin, I. (2002) Climate Res. 21, 1–25.48. Reiter, P. & Darsie, R. F. (1984) Mosquito News 44, 396–399.49. Rogers, D. J. & Randolph, S. E. (2003) Nat. Rev. Microbiol. 1, 231–237.50. Rogers, D. J., Randolph, S. E., Snow, R. W. & Hay, S. I. (2002) Nature 415,

710–715.

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