Skip to main content

Relevant temperatures in mosquito and malaria biology

  • Chapter
Ecology of parasite-vector interactions

Part of the book series: Ecology and control of vector-borne diseases ((ECVD,volume 3))

Abstract

Most biological process-based models that approximate temperature to estimate the various mosquito and parasite life history variables that influence disease transmission intensity. However, mosquitoes, and parasites within them, do not experience ‘average temperatures’, but are exposed to temperatures that can fluctuate considerably throughout the day. In addition, endophilic mosquitoes will be exposed to indoor temperatures and not directly to outdoor air temperature. Further, mosquito larvae live in aquatic habitats and so again, are not exposed directly to outdoor air temperatures. In this chapter we highlight how these different temperatures can all change malaria risk predictions. To understand malaria dynamics, inform operational control objectives and predict consequences of climate change, we need a better mechanistic understanding of vector-parasite interactions, with improved integration of the biological and environmental parameters at a scale relevant to conditions actually experienced by both mosquitoes and malaria parasites.

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

Access this chapter

Chapter
USD 29.95
Price excludes VAT (USA)
  • Available as PDF
  • Read on any device
  • Instant download
  • Own it forever
eBook
USD 129.00
Price excludes VAT (USA)
  • Available as EPUB and PDF
  • Read on any device
  • Instant download
  • Own it forever

Tax calculation will be finalised at checkout

Purchases are for personal use only

Institutional subscriptions

References

  • Afrane YA, Lawson BW, Githeko AK and Yan G (2005) Effects of microclimatic changes caused by land use and land cover on duration of gonotrophic cycles of Anopheles gambiae (Diptera: Culicidae) in western Kenya highlands. J Med Entomol 42: 974-980.

    Article  PubMed  Google Scholar 

  • Afrane YA, Little TJ, Lawson BW, Githeko AK and Yan GY (2008) Deforestation and vectorial capacity of Anopheles gambiae giles mosquitoes in malaria transmission, Kenya. Emerg Infect Dis 14: 1533-1538.

    Article  PubMed  Google Scholar 

  • Afrane YA, Zhou G, Lawson BW, Githeko AK and Yan G (2006) Effects of microclimatic changes caused by deforestation on the survivorship and reproductive fitness of Anopheles gambiae in western Kenya highlands. Am J Trop Med Hyg 74: 772-778.

    PubMed  Google Scholar 

  • Afrane YA, Zhou G, Lawson BW, Githeko AK and Yan G (2007) Life-table analysis of Anopheles arabiensis in western Kenya highlands: effects of land covers on larval and adult survivorship. Am J Trop Med Hyg 77: 660-666.

    PubMed  Google Scholar 

  • Alonso D, Bouma MJ and Pascual M (2011) Epidemic malaria and warmer temperatures in recent decades in an East African highland. Proceedings of the Royal Society B: Biological Sciences 278: 1661-1669.

    Article  PubMed  Google Scholar 

  • Arthurs S, Heinz KM, Thompson S and Krauter PC (2003) Effect of temperature on infection, development and reproduction of the parasitic nematode Thripinema nicklewoodi in Frankliniella occidentalis. Biocontrol 48: 417-429.

    Article  Google Scholar 

  • Atieli H, Menya D, Githeko A and Scott T (2009) House design modifications reduce indoor resting malaria vector densities in rice irrigation scheme area in western Kenya. Malar J 8: 9.

    Article  Google Scholar 

  • Bayoh MN and Lindsay SW (2003) Effect of temperature on the development of the aquatic stages of Anopheles gambiae sensu stricto (Diptera: Culicidae). Bull Entomol Res 93: 375-381.

    Article  PubMed  CAS  Google Scholar 

  • Bødker R, Akida J, Shayo D, Kisinza W, Msangeni HA, Pedersen EM and Lindsay SW (2003) Relationship between altitude and intensity of malaria transmission in the Usambara Mountains, Tanzania. J Med Entomol 40: 706-717.

    Article  PubMed  Google Scholar 

  • Bockarie MJ, Service MW, Barnish G, Maude GH and Greenwood BM (1994) Malaria in a rural area of Sierra Leone. III. Vector ecology and disease transmission. Ann Trop Med Parasitol 88: 251-262.

    Google Scholar 

  • Brière JF, Pracros P, Le Roux AY and Pierre JS (1999) A novel rate model of temperature-dependent development for arthropods. Environ Entomol 28: 22-29.

    Google Scholar 

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

    Article  PubMed  Google Scholar 

  • Christensen JH, Hewitson B, Busuioc A, Chen A, Gao X, Held I, Jones R, Kolli RK, Kwon W-T, Laprise R, Rueda VM, Mearns L, Menéndez CG, Räisänen J, Rinke A, Sarr A and Whetton P (2007) Regional climate projections. In: Solomon S, Qin D, Manning M, Chen Z, Marquis M, Averyt KB, Tignor M and Miller HL (eds.) Climate change 2007: the physical science basis, contribution of working group I to the fourth assessment report of the Intergovernmental Panel on Climate Change. Cambridge University Press, Cambridge, UK, pp. 847-940.

    Google Scholar 

  • Craig MH, Snow RW and Le Sueur D (1999) A climate-based distribution model of malaria transmission in sub-Saharan Africa. Parasitol Today 15: 105-111.

    Article  PubMed  CAS  Google Scholar 

  • Detinova TS (1962) Age-grouping methods in Diptera of medical importance. World Health Organization, Geneva, Switzerland.

    Google Scholar 

  • Dixon AFG, HonÄ›k A, Keil P, Kotela MAA, Å izling AL and Jarošík V (2009) Relationship between the minimum and maximum temperature thresholds for development in insects. Funct Ecol 23: 257-264.

    Article  Google Scholar 

  • Easterling DR, Horton B, Jones PD, Peterson TC, Karl TR, Parker DE, Salinger MJ, Razuvayev V, Plummer N, Jamason P and Folland CK (1997) Maximum and minimum temperature trends for the globe. Science 277: 364-367.

    Article  CAS  Google Scholar 

  • Ebi KL, Hartman J, Chan N, McConnell J, Schlesinger M and Weyant J (2005) Climate suitability for stable malaria transmission in Zimbabwe under different climate change scenarios. Clim Change 73: 375-393.

    Article  Google Scholar 

  • Faye O, Konate L, Mouchet J, Fontenille D, Sy N, Hebrard G and Herve JP (1997) Indoor resting by outdoor biting females of Anopheles gambiae complex (Diptera: Culicidae) in the sahel of northern Senegal. J Med Entomol 34: 285-289.

    PubMed  CAS  Google Scholar 

  • Ferguson HM, Dornhaus A, Beeche A, Borgemeister C, Gottlieb M, Mulla MS, Gimnig JE, Fish D and Killeen GF (2010) Ecology: a prerequisite for malaria elimination and eradication. PLoS Med 7: e1000303.

    Article  PubMed  Google Scholar 

  • Garnham P (1945) Malaria epidemics at exceptionally high altitudes in Kenya. Br Med Bull 2: 456-457.

    Article  Google Scholar 

  • Garnham P (1948) The incidence of malaria at high altitudes. J Nat Mal Soc 7: 275-284.

    CAS  Google Scholar 

  • Geerts B (2003) Empirical estimation of the monthly-mean daily temperature range. Theor Appl Clim 74: 145-165.

    Article  Google Scholar 

  • Giannakou IO, Pembroke B, Gowen SR and Douloumpaka S (1999) Effects of fluctuating temperatures and different host plants on development of Pasteuria penetrans in Meloidogyne javanica. J Nematol 31: 312-318.

    PubMed  CAS  Google Scholar 

  • Gimnig JE, Ombok M, Kamau L and Hawley WA (2001) Characteristics of larval anopheline (Diptera: Culicidae) habitats in western Kenya. J Med Entomol 38: 282-288.

    Article  PubMed  CAS  Google Scholar 

  • Gimnig JE, Ombok M, Otieno S, Kaufman MG, Vulule JM and Walker ED (2002) Density-dependent development of Anopheles gambiae (Diptera: Culicidae) larvae in artificial habitats. J Med Entomol 39: 162-172.

    Article  PubMed  Google Scholar 

  • Githeko AK, Adungo NI, Karanja DM, Hawley WA, Vulule JM, Seroney IK, Ofulla AVO, Atieli FK, Ondijo SO, Genge IO, Odada PK, Situbi PA and Oloo JA (1996a) Some observations on the biting behavior of Anopheles gambiae s.s., Anopheles arabiensis, and Anopheles funestus and their implications for malaria control. Exp Parasitol 82: 306-315.

    Article  PubMed  CAS  Google Scholar 

  • Githeko AK, Service MW, Mbogo CM and Atieli FK (1996b) Resting behaviour, ecology and genetics of malaria vectors in large scale agricultural areas of western Kenya. Parassitologia 38: 481-489.

    Google Scholar 

  • Gotelli N (2001) A primer of ecology. Sinauer Associates, Inc, Sunderlands, MA, USA.

    Google Scholar 

  • Guerra CA, Gikandi PW, Tatem AJ, Noor AM, Smith DL, Hay SI and Snow RW (2008) The limits and intensity of Plasmodium falciparum transmission: Implications for malaria control and elimination worldwide. PLoS Med 5: 300-311.

    Article  Google Scholar 

  • Guerra CA, Howes RE, Patil AP, Gething PW, Van Boeckel TP, Temperley WH, Kabaria CW, Tatem AJ, Manh BH, Elyazar IRF, Baird JK, Snow RW and Hay SI (2010) The international limits and population at risk of Plasmodium vivax transmission in 2009. PLoS Negl Trop Dis 4: e774.

    Article  PubMed  Google Scholar 

  • Harvell CD, Mitchell CE, Ward JR, Altizer S, Dobson AP, Ostfeld RS and Samuel MD (2002) Climate warming and disease risks for terrestrial and marine biota. Science 296: 2158-2162.

    Article  PubMed  CAS  Google Scholar 

  • Highton RB, Bryan JH, Boreham PFL and Chandler JA (1979) Studies on the sibling species Anopheles gambiae Giles and Anopheles arabiensis Patton (Diptera: Culicidae) in the Kisumu area, Kenya. Bull Entomol Res 69: 43-53.

    Article  Google Scholar 

  • Hoshen MB and Morse AP (2004) A weather-driven model of malaria transmission. Malar J 3:32.

    Article  PubMed  Google Scholar 

  • Hulme M, Doherty R, Ngara T, New M and Lister D (2001) African climate change: 1900-2100. Clim Res 17: 145-168.

    Article  Google Scholar 

  • Ikemoto T (2008) Tropical malaria does not mean hot environments. J Med Entomol 45: 963-969.

    Article  PubMed  Google Scholar 

  • Kaufmann O (1932) Some remarks on the influence of temperature fluctuations on the developmental duration and dispersion of insects and its graphical representation by catenary and hyperbola (In German). Z Morphol Ökol Tiere 25: 353-361.

    Article  Google Scholar 

  • Killeen GF, McKenzie FE, Foy BD, Schieffelin C, Billingsley PF and Beier JC (2000) A simplified model for predicting malaria entomologic inoculation rates based on entomologic and parasitologic parameters relevant to control. Am J Trop Med Hyg 62: 535-544.

    PubMed  CAS  Google Scholar 

  • King’uyu SM, Ogallo LA and Anyamba EK (2000) Recent trends of minimum and maximum surface temperatures over eastern Africa. J Clim 13: 2876-2886.

    Article  Google Scholar 

  • Kirby MJ and Lindsay SW (2004) Responses of adult mosquitoes of two sibling species, Anopheles arabiensis and A. gambiae s.s. (Diptera: Culicidae), to high temperatures. Bull Entomol Res 94: 441-448.

    Article  PubMed  CAS  Google Scholar 

  • Kiszewski A, Mellinger A, Spielman A, Malaney P, Sachs SE and Sachs J (2004) A global index representing the stability of malaria transmission. Am J Trop Med Hyg 70: 486-498.

    PubMed  Google Scholar 

  • Kutz SJ, Jenkins EJ, Veitch AM, Ducrocq J, Polley L, Elkin B and Lair S (2009) The Arctic as a model for anticipating, preventing, and mitigating climate change impacts on host-parasite interactions. Vet Parasitol 163: 217-228.

    Article  PubMed  Google Scholar 

  • Lactin DJ, Holliday NJ, Johnson DL and Craigen R (1995) Improved rate model of temperature-dependent development by arthropods. Environ Entomol 24: 68-75.

    Google Scholar 

  • Lafferty KD (2009) Calling for an ecological approach to studying climate change and infectious diseases. Ecology 90: 932-933.

    Article  PubMed  Google Scholar 

  • Lardeux FJ, Tejerina RH, Quispe V and Chavez TK (2008) A physiological time analysis of the duration of the gonotrophic cycle of Anopheles pseudopunctipennis and its implications for malaria transmission in Bolivia. Malar J 7: 17.

    Article  Google Scholar 

  • Lindblade KA, Walker ED, Onapa AW, Katungu J and Wilson ML (2000) Land use change alters malaria transmission parameters by modifying temperature in a highland area of Uganda. Trop Med Int Health 5: 263-274.

    Article  PubMed  CAS  Google Scholar 

  • Lindsay SW, Adiamah JH, Miller JE and Armstrong JRM (1991) Pyrethroid-treated bednet effects on mosquitoes of the Anopheles gambiae complex in The Gambia. Med Vet Entomol 5: 477-483.

    Article  PubMed  CAS  Google Scholar 

  • Lines JD, Myamba J and Curtis CF (1987) Experimental hut trials of permethrin-impregnated mosquito nets and eave curtains against malaria vectors in Tanzania. Med Vet Entomol 1: 37-51.

    Article  PubMed  CAS  Google Scholar 

  • Lobell DB, Bonfils C and Duffy PB (2007) Climate change uncertainty for daily minimum and maximum temperatures: a model inter-comparison. Geo Res Letters 34: 5.

    Google Scholar 

  • Logan JA, Wollkind DJ, Hoyt SC and Tanigoshi LK (1976) An analytic model for description of temperature dependent rate phenomena in arthropods. Environ Entomol 5: 1133-1140.

    Google Scholar 

  • Mahande A, Mosha F, Mahande J and Kweka E (2007) Feeding and resting behaviour of malaria vector, Anopheles arabiensis with reference to zooprophylaxis. Malar J 6: 100.

    Article  PubMed  Google Scholar 

  • Marsh K (2010) Research priorities for malaria elimination. Lancet 376: 1626-1627.

    Article  PubMed  Google Scholar 

  • Martens P, Kovats RS, Nijhof S, de Vries P, Livermore MTJ, Bradley DJ, Cox J and McMichael AJ (1999) Climate change and future populations at risk of malaria. Global Environ Change 9: S89-S107.

    Article  Google Scholar 

  • Mbogo CNM, Baya NM, Ofulla AVO, Githure JI and Snow RW (1996) The impact of permethrin-impregnated bednets on malaria vectors of the Kenyan coast. Med Vet Entomol 10: 251-259.

    Article  PubMed  CAS  Google Scholar 

  • Mnzava AEP, Rwegoshora RT, Wilkes TJ, Tanner M and Curtis CF (1995) Anopheles arabiensis and Anopheles gambiae chromosomal inversion polymorphism, feeding and resting behavior in relation to insecticide house spraying in Tanzania. Med Vet Entomol 9: 316-324.

    Article  PubMed  CAS  Google Scholar 

  • Miller JE, Lindsay SW and Armstrong JRM (1991) Experimental hut trials of bednets impregnated with synthetic pyrethroid or organophosphate insecticide for mosquito control in The Gambia. Med Vet Entomol 5: 465-476.

    Article  PubMed  CAS  Google Scholar 

  • Minakawa N, Omukunda E, Zhou G, Githeko A and Yan G (2006) Malaria vector productivity in relation to the highland environment in Kenya. Am J Trop Med Hyg 75: 448-453.

    PubMed  Google Scholar 

  • Munga S, Minakawa N, Zhou G, Barrack O-OJ, Githeko AK and Yan G (2005) Oviposition site preference and egg hatchability of Anopheles gambiae: effects of land cover types. J Med Entomol 42: 993-997.

    Article  PubMed  Google Scholar 

  • Munga S, Minakawa N, Zhou G, Mushinzimana E, Barrack O-OJ, Githeko AK and Yan G (2006) Association between land cover and habitat productivity of malaria vectors in western Kenyan highlands. Am J Trop Med Hyg 74: 69-75.

    PubMed  Google Scholar 

  • Mutuku FM, Alaii JA, Bayoh MN, Gimnig JE, Vulule JM, Walker ED, Kabiru E and Hawley WA (2006) Distribution, description, and local knowledge of larval habitats of Anopheles gambiae s.l. in a village in western Kenya. Am J Trop Med Hyg 74: 44-53.

    PubMed  Google Scholar 

  • Okech BA, Gouagna LC, Knols BGJ, Kabiru EW, Killeen GF, Beier JC, Yan G and Githure JI (2004a) Influence of indoor microclimate and diet on survival of Anopheles gambiae s.s. (Diptera: Culicidae) in village house conditions in western Kenya. Int J Trop Insect Sci 24: 207-212.

    Article  Google Scholar 

  • Okech BA, Gouagna LC, Walczak E, Kabiru EW, Beier JC, Yan G and Githure JI (2004b) The development of Plasmodium falciparum in experimentally infected Anopheles gambiae (Diptera: Culicidae) under ambient microhabitat temperature in western Kenya. Acta Trop 92: 99-108.

    Article  PubMed  Google Scholar 

  • Paaijmans K, Imbahale S, Thomas M and Takken W (2010a) Relevant microclimate for determining the development rate of malaria mosquitoes and possible implications of climate change. Malar J 9:196.

    Article  PubMed  Google Scholar 

  • Paaijmans KP, Blanford S, Bell AS, Blanford JI, Read AF and Thomas MB (2010b) Influence of climate on malaria transmission depends on daily temperature variation. Proc Natl Acad Sci USA 107: 15135-15139.

    Article  PubMed  CAS  Google Scholar 

  • Paaijmans KP, Huijben S, Githeko AK and Takken W (2009a) Competitive interactions between larvae of the malaria mosquitoes Anopheles arabiensis and Anopheles gambiae under semi-field conditions in western Kenya. Acta Trop 109: 124-130.

    Article  PubMed  Google Scholar 

  • Paaijmans KP, Jacobs AFG, Takken W, Heusinkveld BG, Githeko AK, Dicke M and Holtslag AAM (2008) Observations and model estimates of diurnal water temperature dynamics in mosquito breeding sites in western Kenya. Hydrol Proc 22: 4789-4801.

    Article  Google Scholar 

  • Paaijmans KP, Read AF and Thomas MB (2009b) Understanding the link between malaria risk and climate. Proc Natl Acad Sci USA 106: 13844-13849.

    Article  PubMed  CAS  Google Scholar 

  • Parham PE and Michael E (2010) Modeling the effects of weather and climate change on malaria transmission. Environ Health Perspect 118: 620-626.

    Article  PubMed  Google Scholar 

  • Parton WJ and Logan JA (1981) A model for diurnal variation in soil and air temperature. Agr Met 23: 205-216.

    Article  Google Scholar 

  • Pascual M, Ahumada JA, Chaves LF, Rodó X and Bouma M (2006) Malaria resurgence in the East African highlands: temperature trends revisited. Proc Natl Acad Sci USA 103: 5829-5834.

    Article  PubMed  CAS  Google Scholar 

  • Pascual M, Dobson AP and Bouma MJ (2009) Underestimating malaria risk under variable temperatures. Proc Natl Acad Sci USA 106: 13645-13646.

    Article  PubMed  CAS  Google Scholar 

  • Patz JA and Olson SH (2006) Malaria risk and temperature: Influences from global climate change and local land use practices. Proc Natl Acad Sci USA 103: 5635-5636.

    Article  PubMed  CAS  Google Scholar 

  • Rogers DJ and Randolph SE (2000) The global spread of malaria in a future, warmer world. Science 289: 1763-1766.

    Article  PubMed  CAS  Google Scholar 

  • Rogers DJ and Randolph SE (2006) Climate change and vector-borne diseases. In: Hay SI, Graham A and Rogers DJ (eds.) Global mapping of infectious diseases: methods, examples and emerging applications (Advances in Parasitology), Elsevier, San Diego, CA, USA, pp. 345-381.

    Google Scholar 

  • Rúa GL, Quiñones ML, Vélez ID, Zuluaga JS, Rojas W, Poveda G and Ruiz D (2005) Laboratory estimation of the effects of increasing temperatures on the duration of gonotrophic cycle of Anopheles albimanus (Diptera: Culicidae). Mem Inst Oswaldo Cruz 100: 515-520.

    Article  PubMed  Google Scholar 

  • Ruel JJ and Ayres MP (1999) Jensen’s inequality predicts effects of environmental variation. Trends Ecol Evol 14: 361-366.

    Article  PubMed  Google Scholar 

  • Ruissen MA, Vandervossen RTM and Kocks CG (1993) Growth of Xanthomonas campestris pv. campestris populations at constant and variable temperatures. Neth J Plant Path 99: 173-179.

    Article  Google Scholar 

  • Scherm H and Van Bruggen AHC (1994) Effects of fluctuating temperatures on the latent period of lettuce downy mildew (Bremia lactucae). Phytopathology 84: 853-859.

    Article  Google Scholar 

  • Service MW (1970) Ecological notes on species A and B of the Anopheles gambiae complex in the Kisumu area of Kenya. Bull Entomol Res 60: 105-108.

    Article  Google Scholar 

  • Service MW, Joshi GP and Pradhan GD (1978) Survey of Anopheles gambiae (species A) and An. arabiensis (species B) of An. gambiae Giles complex in the Kisumu area of Kenya following insecticidal spraying with OMS-43 (Fenitrothion). Ann Trop Med Parasitol 72: 377-386.

    Google Scholar 

  • Studer A, Thieltges DW and Poulin R (2010) Parasites and global warming: net effects of temperature on an intertidal host-parasite system. Mar Ecol Prog Ser 415: 11-22.

    Article  Google Scholar 

  • Worner SP (1992) Performance of phenological models under variable temperature regimes: consequences of the Kaufmann or rate summation effect. Environ Entomol 21: 689-699.

    Google Scholar 

  • Xu XM (1996) The effects of constant and fluctuating temperatures on the length of the incubation period of apple powdery mildew (Podosphaera leucotricha). Plant Pathol 45: 924-932.

    Article  Google Scholar 

Download references

Acknowledgements

This project was supported by a Netherlands Organisation for Scientific Research (NWO) grant and a NSF-EID program grant (#EF-0914384).

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to Krijn P. Paaijmans .

Rights and permissions

Reprints and permissions

Copyright information

© 2013 Wageningen Academic Publishers The Netherlands

About this chapter

Cite this chapter

Paaijmans, K.P., Thomas, M.B. (2013). Relevant temperatures in mosquito and malaria biology. In: Ecology of parasite-vector interactions. Ecology and control of vector-borne diseases, vol 3. Wageningen Academic Publishers, Wageningen. https://doi.org/10.3920/978-90-8686-744-8_5

Download citation

Publish with us

Policies and ethics