Abstract
Knowledge of the interrelationship of mosquito communities and land use changes is of paramount importance to understand the potential risk of mosquito disease transmission. This study examined the effects of land use types in urban, peri-urban and natural landscapes on mosquito community structure to test whether the urban landscape is implicated in increased prevalence of potentially harmful mosquitoes. Three land use types (park, farm, and forest nested in urban, peri-urban and natural landscapes, respectively) in Klang Valley, Malaysia, were surveyed for mosquito larval habitat, mosquito abundance and diversity. We found that the nature of human activities in land use types can increase artificial larval habitats, supporting container-breeding vector specialists such as Aedes albopictus, a dengue vector. In addition, we observed a pattern of lower mosquito richness but higher mosquito abundance, characterised by the high prevalence of Ae. albopictus in the urban landscape. This was also reflected in the mosquito community structure whereby urban and peri-urban landscapes were composed of mainly vector species compared to a more diverse mosquito composition in natural landscape. This study suggested that good environmental management practices in the tropical urban landscape are of key importance for effective mosquito-borne disease management.
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References
Abdullah SA, Hezri AA (2008) From forest landscape to agricultural landscape in the developing tropical country of Malaysia: pattern, process, and their significance on policy. Environmental Management 42:907-917
Bates D, Maechler M, Bolker B, Walker S (2015) Fitting linear mixed-effects model using lme4. Journal of Statistical Software 67:1-48
Berakhi RO, Oyana TJ, Adu-Prah S (2015) Land use and land cover change and its implications in Kagera river basin, East Africa. African Geographical Review 34:209-231
Bonizzoni M, Gasperi G, Chen X, James AA (2013) The invasive mosquito species Aedes albopictus: current knowledge and future perspective. Trends in Parasitology 29:460-468
Bulleri F, Benedetti-Cecchi L, Jaklin A, Lvesa L (2016) Linking disturbance and resistance to invasion via changes in biodiversity: a conceptual model and an experimental test on rocky reefs. Ecology and Evolution 6:2010-2021
Chen DC, Lee HL, Lau KW, Abdullah AG, Tan SB, Sa’diyah I, Norma-Rashid Y, Oh PF, Chan CK, Sofian-Azirun M (2014a) Biting behaviour of Malaysian mosquitoes, Aedes albopictus Skuse, Armigeres kesseli Ramalingam, Culex quinquefasciatus Say, and Culex vishnui Theobald obtained from urban residential areas in Kuala Lumpur. Asian Biomedicine 8:315-321
Chen X, Wang W, Liang H, Liu X, Da L (2014b) Dynamics of ruderal species diversity under the rapid urbanisation over the past half century in Harbin, Northeast China. Urban Ecosystems 17:455-472
Cheong YL, Leitao PJ, Lakes T (2014) Assessment of land use factors associated with dengue cases in Malaysia using boosted regression trees. Spatial and Spatio-temporal Epidemiology 10:75-84
Clarke KR, Gorley RN (2006) Primer v6: user manual/tutorial. PRIMER-E, Plymouth
Despommier D, Ellis BR, Wilcox BA (2006) The role of ecotones in emerging infectious diseases. EcoHealth 3:281-289
Fedele G, Locatelli B, Djoudi H, Colloff MJ (2018) Reducing risk by transforming landscapes: Cross-scale effects of land-use changes on ecosystem services. PLoS ONE 13:e0195895
Fick S, Hijmans R (2017) Worldclim 2: New 1-km spatial resolution climate surfaces for global land areas. International Journal of Climatology 37:4302–4315
Friggens MM, Beler P (2010) Anthropogenic disturbance and the risk of flea-borne disease transmission. Oecologia 164:809–820
Gaertner M, Wilson JRU, Cadotte MW, Macivor S, Zenni RD, Richardson DM (2017) Non-native species in urban environments: patterns, processes, impacts and challenges. Biological Invasions 19:3461-3469
Galvani A, Bauch CT, Anand M, Singer BH, Levin SA (2016) Human-environment interactions in population and ecosystem health. Proceedings of the National Academy of Sciences of the United States of America 113:14502-14506
Gibbs HK, Ruesch AS, Achard F, Clayton MK, Holmgren P, Ramankutty N, Foley JA (2010) Tropical forests were the primary sources of new agricultural land in the 1980s and 1990s. Proceedings of the National Academy of Sciences of the United States of America 107:16732-16737
Gottdenker N, Streicker D, Faust CL, Carroll R (2014) Anthropogenic land use change and infectious diseases: a review of the evidence. EcoHealth 11:619-632
Griswold MW, Lounibos LP (2005) Competitive outcomes of aquatic container Diptera depend on predation and resource levels. Annals of the Entomological Society of America 98:673-681
Gubler DJ (2011) Dengue, urbanization and globalization. Tropical Medicine and Health 39(4 Suppl):3-11
Guo F, Bonebrake TC, Gibson L (2018) Land-use change alters host and vector communities and may elevate disease risk. EcoHealth. https://doi.org/10.1007/s10393-018-1336-3 [Online 24 April, 2018]
Hassan H, Shohaimi S, Hashim NR (2012) Risk mapping of dengue in Selangor and Kuala Lumpur, Malaysia. Geospatial Health 7:21-25
Hassell JM, Begon M, Ward MJ, Fevre EM (2017) Urbanisation and disease emergence: dynamics at the wildlife-livestock-human interface. Trends in Ecology & Evolution 32:55-67
Hidalgo K, Siaussat D, Braman V, Dabire KR, Simard F, Mouline K, Renault D (2016) Comparative physiological plasticity to desiccation in distinct populations of the malarial mosquito Anopheles coluzzii. Parasites & Vectors 9:565
Holway DA, Suarez A (2006) Homogenization of ant communities in mediterranean California: the effects of urbanisation and invasion. Biological Conservation 127:319-326
Jeffery J, Rohela M, Muslimin M, Abdul Aziz SMN, Jamaiah I, Kumar S, Tan TC, Lim YAL, Nissapatorn V, Abdul-Aziz NM (2012) Illustration keys: some mosquitoes of Peninsula Malaysia, Kuala Lumpur: University of Malaya Press
Joanne S, Vythilingam I, Teoh BT, Leong CS, Tan KK, Wong ML, Yugavathy N, AbuBakar S (2017) Vector competence of Malaysian Aedes albopictus with and without Wolbachia to four dengue virus serotypes. Tropical Medicine & International Health 22:1154-1165
Kesavaraju B, Damal K, Juliano SA (2008) Do natural container habitats impede invader dominance? Predator-mediated coexistence of invasive and native container-dwelling mosquitoes. Oecologia 155:631-639
Kilpatrick, AM (2011) Globalization, land use, and the invasion of West Nile virus. Science 334:213-220
Kunz Y, Steinbach S, Dittrich C, Hauser-Schaublin B, Rosyani I, Soetarto E, Faust H. (2017) ‘The fridge in the forest’: historical trajectories of land tenure regulations fostering landscape transformation in Jambi Province, Sumatra, Indonesia. Forest Policy and Economics 81:1-9
Lam K-C, Ng S, Hui W-C, Chan PK (2005) Environmental quality of urban parks and open spaces in Hong Kong. Environmental Monitoring and Assessment 111:55-73
Lambin EF, Meyfroidt P (2011) Global land use change, economic globalization, and the looming land scarcity. Proceedings of the National Academy of Sciences of the United States of America 108:3465-3472
Le Menach AL, Mckenzie FE, Flahault A, Smith DL (2005) The unexpected importance of mosquito oviposition behaviour for malaria: non-productive larval habitats can be sources for malaria transmission. Malaria Journal 4:23
Lempp C, Jungwirth N, Grilo ML, Reckendorf A, Ulrich A, van Neer A, Bodewes R, Pfankuche, VM, Bauer C, Osterhaus ADME, Baumgartner W, Siebert U (2017) Pathological findings in the red fox (Vulpes vulpes), stone marten (Martes foina) and raccoon dog (Nyctereutes procyonoides), with special emphasis on infectious and zoonotic agents in Northern Germany. PLoS ONE 12:e0175469
Li Y, Kamara F, Zhou G, Puthiyakunnon S, Li C, Liu Y, Zhou Y, Yao L, Yan G, Chen X (2014) Urbanisation increases Aedes albopictus larval habitats and accelerates mosquito development and survivorship. PLoS Neglected Tropical Diseases 8:e3301
Liew C, Curtis CF (2004) Horizontal and vertical dispersal of dengue vector mosquitoes, Aedes aegypti and Aedes albopictus, in Singapore. Medical and Veterinary Entomology 18:351-360
Lopez-Carr D, Burgdorfer J (2013) Deforestation drivers: population, migration, and tropical land use. Environment Science and Policy for Sustainable Development 55:3-11
Martinuzzi S, Gould WA, Ramos Gonzalez OM (2007) Land development, land use, and urban sprawl in Puerto Rico integrating remote sensing and population census data. Landscape and Urban Planning 79:288-297
McKinney ML (2008) Effects of urbanisation on species richness: a review of plants and animals. Urban Ecosystems 11:161-176
Meador MR, Coles JF, Zappia H (2005) Fish assemblage responses to urban intensity gradients in contrasting metropolitan areas: Birmingham, Alabama and Boston, Massachusetts In: Effects of Urbanisation on Stream Ecosystems, American Fisheries Society Symposium, Brown LR, Gray RH, Hughes RM, Meador MR (editors), pp 409–423
Meyer Steiger DB, Ritchie SA, Laurance, SG (2016) Mosquito communities and disease risk influenced by land use change and seasonality in the Australian tropics. Parasites & Vectors 9:387
Midega JT, Smith DL, Olotu A, Mwangangi JM, Nzovu JG, Wambua J, Nyangweso G, Mbogo CM, Christophides GK, Marsh K, Bejon P (2012) Wind direction and proximity to larval sites determines malaria risk in Kilifi district in Kenya. Nature Communications 3:674
Nagendra H, Gopal D (2011) Tree diversity, distribution, history and change in urban parks: studies in Bangalore, India. Urban Ecosystems 12:211-223
Nor Akmar AA, Konijnendijk CC, Sreetheran M, Nilsson K (2011) Greenspace planning and management in Klang Valley, Peninsular Malaysia. Arboriculture and Urban Forestry 37:99-107
Ochola GO (2018) Natural resource use dilemma: a review of effects of population growth on natural resources in Kenya. International Journal of Environmental Sciences & Natural Resources 13:1-4
Patz J, Daszak P, Tabor GM, Alonso Aguirre A, Pearl M, Epstein J, Wolfe ND, Marm Kilpatrick A, Foufopoulos J, Molyneux D, Bradley DJ (2004) Unhealthy landscape: policy recommendations on land use change and infectious disease emergence. Environmental Health Perspectives 112:1092-1098
Potchter O, Cohen P, Bitan A (2006) Climatic behavior of various urban parks during hot and humid summer in the Mediterranean city of Tel Aviv, Israel. International Journal of Climatology 26:1695-1711
Rattanarithikul R, Harbach RE, Harrison BA, Panthusiri P, Jones JW, Coleman RE (2005) Illustrated keys to the mosquitoes of Thailand. II. Genera Culex and Lutzia. Southeast Asian Journal of Tropical Medicine 36:1-97
Rattanarithikul R, Harrison BA, Panthusiri P, Peyton EL, Coleman RE (2006) Illustrated keys to the mosquitoes of Thailand III. Genera Aedeomyia, Ficalbia, Mimomyia, Hodgesia, Coquillettidia, Mansonia, and Uranotaenia. Southeast Asian Journal Tropical Medicine 37:1-85
Rattanarithikul R, Harbach RE, Harrison BA, Panthusiri P, Coleman RE (2007) Illustrated keys to the mosquitoes of Thailand V. Genera Orthopodomyia, Kimia, Malaya, Topomyia, Tripteroides, and Toxorhynchites. Southeast Asian Journal Tropical Medicine 38:1-65
Rattanarithikul R, Harbach RE, Harrison BA, Panthusiri P, Coleman RE, Richardson JH (2010). Illustrated keys to the mosquitoes of Thailand. VI. Tribe Aedini. Southeast Asian Journal Tropical Medicine 41:1-225
Riley SPD, Busteed GT, Kats LB, Vandergon TL, Lee LFS, Dagit RG, Kerby JL, Fisher RN, Sauvajot RM (2005) Effects of urbanisation on the distribution and abundance of amphibians and invasive species in Southern California. Conservation Biology 19:1894-1907
Robson JP, Berkes F (2011) Exploring some of the myths of land use change: can rural to urban migration drive declines in biodiversity? Global Environmental Change 21:844-854
Rozilawati H, Taneselvi K, Nazni WA, Mohd Masri S, Zairi J, Adanan CR, Lee HL (2015) Surveillance of Aedes albopictus Skuse breeding preference in selected dengue outbreak localities, Peninsular Malaysia. Tropical Biomedicine 32:49-64
Ryan SJ, Carlson CJ, Mordecai EA, Johnson LR (2019) Global expansion and redistribution of Aedes-borne virus transmission risk with climate change. PLoS Neglected Tropical Diseases 13:e0007231
Saleeza SN, Norma-Rashid Y, Azirun MS (2013) Mosquito species and outdoor breeding places in residential areas in Malaysia. Southeast Asian Journal of Tropical Medicine and Public Health 44:963-969.
Schielein J, Borner J (2018) Recent transformations of land-use and land-cover dynamics across different deforestation frontiers in the Brazilian Amazon. Land Use Policy 76:81-94
Schneider UA, Havlik P, Schmid E, Valin H, Mosnier A, Obersteiner M, Bottcher H, Skalsky R, Balkovic J, Sauer T, Fritz S (2011) Impacts of population growth, economic development, and technical change on global food production and consumption. Agricultural Systems 104:204-215
Seto KC, Guneralp B, Hutyra LR (2012) Global forecasts of urban expansion to 2030 and direct impacts on biodiversity and carbon pools. Proceedings of the National Academy of Sciences of the United States of America 109:16083-16088
Shochat E, Lerman SB, Anderies JM, Warren PS, Faeth SH, Nilon CH (2010) Invasion, competition, and biodiversity loss in urban ecosystems. Bioscience 60:199-208
Sibley CG, Liu, JH (2003) Differentiating active and passive littering: a two-stage process model of littering behavior in public spaces. Environment and Behavior 35:415-533
Smith DL, Dushoff J, McKenzie, FE (2004) The risk of a mosquito-borne infection in a heterogeneous environment. PLoS Biology 2:e368
Stein A, Gerstner K, Kreft H (2014) Environmental heterogeneity as a universal driver of species richness across tax, biomes and spatial scales. Ecology Letters 17:866-880
Thongsripong P, Green A, Kittayapong P, Kapan D, Wilcox B, Bennett S (2013) Mosquito vector diversity across habitats in central Thailand endemic for dengue and other arthropod-borne diseases. PLoS Neglected Tropical Diseases 7:e2507
Toure SI, Stow DA, Clarke K, Weeks J (2018) Patterns of land cover and land use change within the two major metropolitan areas of Ghana. Geocarto International. https://doi.org/10.1080/10106049.2018.1516244 [Online 1 October, 2018]
Turok I, McGranahan G (2013) Urbanisation and economic growth: the arguments and evidence for Africa and Asia. Environment and Urbanisation 25:465-482
Vasilakis N, Cardosa J, Hanley KA, Holmes EC, Weaver SC (2011) Fever from the forest: prospects for the continued emergence of sylvatic dengue virus and its impact on public health. Nature 9:532-541
Villegas Vallejos MA, Padial AA, Vitule JRS (2016) Human-induced landscape changes homogenize Atlantic forest bird assemblages through nested species loss. PLoS ONE 11:e0147058
von Dohren P, Haase D (2015) Ecosystem disservices research: a review of the state of the art with a focus on cities. Ecological Indicators 52:490-497
Wells K, Lakim MB, O’Hara RB (2014) Shift from native to invasive small mammals across gradients from tropical forest to urban habitat in Borneo. Biodiversity and Conservation 23:289-2303
Western D (2001) Human-modified ecosystems and future evolution. Proceedings of the National Academy of Sciences of the United States of America 98:5458-5465
Wiens JJ, Ackerly DD, Allen AP, Anacker BL, Buckley LB, Cornell HV, Damschen EI, Jonathan Davies T, Grytnes JA, Harrison SP, Hawkins BA, Holt RD, McCain CM, Stephens PR (2010) Niche conservation as an emerging principle in ecology and conservation biology. Ecology Letters 13:1310-1324
World Health Organisation (2014) A global brief on vector-borne diseases. Geneva: WHO
Zahouli JBZ, Koudou BG, Muller P, Malone D, Tano Y, Utzinger J (2017) Effect of land-use changes on the abundance, distribution, and host-seeking behaviour of Aedes arbovirus vectors in oil palm-dominated landscapes, southeastern Cote d’Ivoire. PLoS ONE 12:e0189082
Acknowledgements
This work was part of the research for Ph.D. by LJM at Monash University Malaysia (MUM) funded by Tropical Medicine and Biology Platform to RS, School of Science PhD fellowship to LJM and School of Science Seed Grant to YSH.
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Lee, J.M., Wasserman, R.J., Gan, J.Y. et al. Human Activities Attract Harmful Mosquitoes in a Tropical Urban Landscape. EcoHealth 17, 52–63 (2020). https://doi.org/10.1007/s10393-019-01457-9
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DOI: https://doi.org/10.1007/s10393-019-01457-9