Skip to main content
SpringerLink
Log in

Forest Restoration and the Zoonotic Vector Anopheles balabacensis in Sabah, Malaysia

  • Original Contribution
  • Published:
EcoHealth Aims and scope Submit manuscript

Abstract

Anthropogenic changes to forest cover have been linked to an increase in zoonotic diseases. In many areas, natural forests are being replaced with monoculture plantations, such as oil palm, which reduce biodiversity and create a mosaic of landscapes with increased forest edge habitat and an altered micro-climate. These altered conditions may be facilitating the spread of the zoonotic malaria parasite Plasmodium knowlesi in Sabah, on the island of Borneo, through changes to mosquito vector habitat. We conducted a study on mosquito abundance and diversity in four different land uses comprising restored native forest, degraded native forest, an oil palm estate and a eucalyptus plantation, these land uses varying in their vegetation types and structure. The main mosquito vector, Anopheles balabacensis, has adapted its habitat preference from closed canopy rainforest to more open logged forest and plantations. The eucalyptus plantations (Eucalyptus pellita) assessed in this study contained significantly higher abundance of many mosquito species compared with the other land uses, whereas the restored dipterocarp forest had a low abundance of all mosquitos, in particular, An. balabacensis. No P. knowlesi was detected by PCR assay in any of the vectors collected during the study; however, P. inui, P. fieldi and P. vivax were detected in An. balabacensis. These findings indicate that restoring degraded natural forests with native species to closed canopy conditions reduces abundance of this zoonotic malarial mosquito vector and therefore should be incorporated into future restoration research and potentially contribute to the control strategies against simian malaria.

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

Figure 1
Figure 2
Figure 3
Figure 4
Figure 5

Similar content being viewed by others

References

  • Afrane YA, Lawson BW, Githeko AK, 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. Journal of Medical Entomology 42:974–980

    Article  PubMed  Google Scholar 

  • Afrane YA, Zhou G, Lawson BW, Githeko AK, Yan G (2007) Life-table analysis of anopheles Arabiensis in Western Kenya Highlands: Effects of land covers on larval and adult survivorship. The American Journal of Tropical Medicine and Hygiene 77:660–666

    Article  PubMed  Google Scholar 

  • Agyekum TP, Botwe PK, Arko-Mensah J, Issah I, Acquah AA, Hogarh JN, Dwomoh D, Robins TG, Fobil JN (2021) A systematic review of the effects of temperature on anopheles mosquito development and survival: Implications For Malaria control in a future warmer climate. International Journal of Environmental Research and Public Health 18:7255

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Alloysius, D., Falck, J., Wai, Y. & Karlsson, A. 2010. An attempt to rehabilitate a degraded tropical rainforest in Borneo: the biological results and the social benefits of the ikea investment, an analysis after Ten Years. In Proceedings Of Xxiii Iufro World Congress 2010.

  • Ang JXD, Kadir KA, Mohamad DSA, Matusop A, Divis PCS, Yaman K, Singh B (2020) New vectors in Northern Sarawak, Malaysian Borneo, for the zoonotic Malaria Parasite. P. Knowlesi. Parasites & Vectors 13:472

    Article  Google Scholar 

  • Ashton MS, Gunatilleke C, Singhakumara B, Gunatilleke I (2001) Restoration pathways for rain forest in Southwest Sri Lanka: A review of concepts and models. Forest Ecology and Management 154:409–430

    Article  Google Scholar 

  • Aure WE, Salazar NP, Chua TH (2021) Larval ecology of anopheles mosquitoes in Kudat Sabah. Borneo Journal of Medical Sciences (bjms) 49:62

    Google Scholar 

  • Banin LF, Raine EH, Rowland LM, Chazdon RL, Smith SW, Rahman NEB, Butler A, Philipson C, Applegate GG, Axelsson EP (2023) The Road To recovery: A synthesis of outcomes from ecosystem restoration in tropical and Sub-Tropical Asian forests. Philosophical Transactions of the Royal Society B 378:20210090

    Article  Google Scholar 

  • Brancalion PH, Niamir A, Broadbent E, Crouzeilles R, Barros FS, Almeyda Zambrano AM, Baccini A, Aronson J, Goetz S, Reid JL (2019) Global restoration opportunities in tropical rainforest landscapes. Science Advances 5:eaav223

    Article  Google Scholar 

  • Brant HL, Ewers RM, Vythilingam I, Drakeley C, Benedick S, Mumford JD (2016) Vertical stratification of adult mosquitoes (Diptera: Culicidae) within a tropical rainforest in Sabah. Malaysia. Malaria Journal 15:370

    Article  PubMed  Google Scholar 

  • Bray JR, Curtis JT (1957) An ordination of the upland forest communities of southern Wisconsin. Ecological Monographs 27:326–349

    Article  Google Scholar 

  • Brown R, Ferguson H, Salgado-Lynn M, Tock-Hing C, Vythilingam I, Jumail A, Jalius C (2021) Measuring the exposure of primate reservoir hosts to mosquito vectors in Malaysian Borneo. Biorxiv. 2:1186

    Google Scholar 

  • Burraco P, Iglesias-Carrasco M, Cabido C, Gomez-Mestre I (2018) Eucalypt leaf litter impairs growth and development of Amphibian Larvae, inhibits their antipredator responses and alters their physiology. Conservation Physiology 6:Coy066

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Byrne I, Aure W, Manin BO, Vythilingam I, Ferguson HM, Drakeley CJ, Chua TH, Fornace KM (2021) Environmental and spatial risk factors for the larval habitats of P. knowlesi vectors in Sabah, Malaysian Borneo. Scientific Reports 11:1–11

    Article  Google Scholar 

  • Chang M, Hii J, Buttner P, Mansoor F (1997) Changes in abundance and behaviour of vector mosquitoes induced by land use during the development of an oil palm plantation in Sarawak. Transactions of the Royal Society of Tropical Medicine and Hygiene 91:382–386

    Article  CAS  PubMed  Google Scholar 

  • Chin AZ, Avoi R, Atil A, Lukman KA, Rahim SSA, Ibrahim MY, Ahmed K, Jeffree MS (2021) Risk factor of P. knowlesi infection In Sabah Borneo Malaysia, 2020: A population-based case-control study. PLOS ONE 16(9):e0257104. https://doi.org/10.1371/journal.pone.0257104

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Chua TH, Manin BO, Daim S, Vythilingam I, Drakeley C (2017) Phylogenetic analysis of simian Plasmodium spp infecting anopheles balabacensis baisas in Sabah Malaysia. PLOS Neglected Tropical Diseases 11:e0005991

    Article  PubMed  PubMed Central  Google Scholar 

  • Chua TH, Manin BO, Vythilingam I, Fornace K, Drakeley CJ (2019) Effect of different habitat types on abundance and biting times of anopheles Balabacensis Baisas (Diptera: Culicidae) in Kudat District of Sabah, Malaysia. Parasites & Vectors 12:1–13

    Article  Google Scholar 

  • Chua TH, Manin BO, Fornace K (2022) Life table analysis of anopheles Balabacensis, the primary vector of P. knowlesi in Sabah. Malaysia. Parasites & Vectors 15:442

    Article  Google Scholar 

  • Clarke, K. R., Gorley, R. N., Somerfield, P. J. & Warwick, R. M. 2014. Change in marine communities: An approach to statistical analysis and interpretation.

  • Cooper DJ, Rajahram GS, William T, Jelip J, Mohammad R, Benedict J, Alaza DA, Malacova E, Yeo TW, Grigg MJ (2020) Plasmodium knowlesi Malaria in Sabah, Malaysia, 2015–2017: Ongoing increase in incidence despite near-elimination of the human-only plasmodium species. Clinical Infectious Diseases 70:361–367

    Article  PubMed  Google Scholar 

  • Cosset CCP, Edwards DP (2017) The effects of restoring logged tropical forests on avian phylogenetic and functional diversity. Ecological Applications 27:1932–1945

    Article  PubMed  Google Scholar 

  • Cousins SH (1991) Species diversity measurement: choosing the right index. Trends in Ecology & Evolution 6:190–192

    Article  CAS  Google Scholar 

  • Crespo Mingueza L (2018) Presence AND Habitat Use of the Endangered Bornean Elephant (Elephas Maximus Borneensis) in the Inikea Rehabilitation Project Site. Malaysia: Sabah

    Google Scholar 

  • Dewald JR, Fuller DO, Müller GC, Beier JC (2016) A novel method for mapping village-scale outdoor resting microhabitats of the primary African Malaria Vector, Anopheles Gambiae. Malaria Journal 15:1–12

    Article  Google Scholar 

  • Edwards D, Backhouse A, Wheeler C, Khen C, Hamer K (2012) Impacts of logging and rehabilitation on invertebrate communities in tropical rainforests of Northern Borneo. Journal of Insect Conservation 16:591–599

    Article  Google Scholar 

  • Elliott, S. D., Blakesley, D. & Hardwick, K. 2013. Restoring tropical forests: A Practical Guide., Kew, Royal Botanic Gardens.

  • Ellis, M. R. & Ladeau, S. 2013. Influence of dragonfly larvae on mosquito development and survival. Cary Institute Of Ecosystem Studies, 1–7.

  • Fornace KM, Herman LS, Abidin TR, Chua TH, Daim S, Lorenzo PJ, Grignard L, Nuin NA, Ying LT, Grigg MJ (2018) Exposure and infection to P. knowlesi in case study communities in Northern Sabah, Malaysia and Palawan. The Philippines. Plos Neglected Tropical Diseases 12:E0006432

    Article  PubMed  Google Scholar 

  • Fornace KM, Brock PM, Abidin TR, Grignard L, Herman LS, Chua TH, Daim S, William T, Patterson CL, Hall T (2019) Environmental risk factors and exposure to the Zoonotic Malaria Parasite P. knowlesi across northern Sabah, Malaysia: A population-based cross-sectional Survey. The Lancet Planetary Health 3:E179–E186

    Article  PubMed  PubMed Central  Google Scholar 

  • Gaveau DL, Locatelli B, Salim MA, Yaen H, Pacheco P, Sheil D (2019) Rise and fall of forest loss and industrial plantations in Borneo (2000–2017). Conservation Letters 12:e12622

    Article  Google Scholar 

  • Gornish, E. S., Mccormick, M., Begay, M. & Nsikani, M. M. 2021. Sharing knowledge to improve ecological restoration outcomes. Restoration Ecology, E13417.

  • Gouagna LC, Rakotondranary M, Boyer S, Lempérière G, Dehecq J-S, Fontenille D (2012) Abiotic and biotic factors associated with the presence of anopheles Arabiensis immatures and their abundance in naturally occurring and man-made aquatic habitats. Parasites & Vectors 5:96

    Article  Google Scholar 

  • Gregory N, Ewers RM, Chung AYC, Cator LJ (2019) El Niño drought and tropical forest conversion synergistically determine mosquito development rate. Environmental Research Letters 14:35003

    Article  Google Scholar 

  • Grieco JP, Achee NL, Briceno I, King R, Andre R, Roberts D, Rejmankova E (2003) Comparison of life table attributes from newly established colonies of anopheles albimanus and anopheles vestitipennis in Northern Belize. Journal of Vector Ecology 28:200–207

    PubMed  Google Scholar 

  • Grignard L, Shah S, Chua TH, William T, Drakeley CJ, Fornace KM (2019) Natural human infections with P. cynomolgi and other malaria species in an elimination setting In Sabah, Malaysia. The Journal of Infectious Diseases 220:1946–1949

    Article  PubMed  PubMed Central  Google Scholar 

  • Hardwick SR, Toumi R, Pfeifer M, Turner EC, Nilus R, Ewers RM (2015) The relationship between leaf area index and microclimate in tropical forest and oil palm plantation: Forest disturbance drives changes in microclimate. Agricultural and Forest Meteorology 201:187–195

    Article  ADS  PubMed  PubMed Central  Google Scholar 

  • Hawkes FM, Manin BO, Cooper A, Daim S, Jelip J, Husin T, Chua TH (2019) Vector compositions change across forested to deforested ecotones in emerging areas of zoonotic malaria transmission in Malaysia. Scientific Reports 9:1–12

    Google Scholar 

  • Hod R, Mokhtar SA, Muharam FM, Shamsudin UK, HishamHashim J (2022) Developing a predictive model for P. knowlesi susceptible areas in Malaysia using geospatial data and artificial neural networks. Asia Pacific Journal of Public Health 34:182–190

    Article  PubMed  Google Scholar 

  • Holl KD (2017) Restoring tropical forests from the bottom up. Science 355:455

    Article  ADS  CAS  PubMed  Google Scholar 

  • Hutcheson K (1970) A test for comparing diversities based on the Shannon Formula. Journal of Theoretical Biology 29:151–154

    Article  ADS  CAS  PubMed  Google Scholar 

  • Iglesias-Carrasco M, Cabido C, Ord TJ (2022) Natural toxins leached from eucalyptus Globulus plantations affect the development and life-history of Anuran tadpoles. Freshwater Biology 67:378–388

    Article  CAS  Google Scholar 

  • Jayaraj VJ, Baharaja D, Gopalakrishnan N, Kaco Y (2017) Locally Transmitted Malaria in Tawau, Sabah. Malaysia: Malariaworld Journal, p 8

    Google Scholar 

  • Jeyaprakasam NK, Liew JWK, Low VL, Wan-Sulaiman W-Y, Vythilingam I (2020) Plasmodium knowlesi infecting humans in Southeast Asia: What’s next? Plos Neglected Tropical Diseases 14:e0008900

    Article  PubMed  PubMed Central  Google Scholar 

  • Jeyaprakasam NK, Low VL, Liew JWK, Pramasivan S, Wan-Sulaiman W-Y, Saeung A, Vythilingam I (2022) Blood meal analysis of anopheles vectors of simian Malaria based on laboratory and field studies. Scientific Reports 12:1–13

    Article  Google Scholar 

  • Jiram AI, Vythilingam I, Noorazian YM, Yusof YM, Azahari AH, Fong M-Y (2012) Entomologic investigation of P. knowlesi vectors in Kuala Lipis, Pahang Malaysia. Malaria Journal 11:213

    Article  PubMed  PubMed Central  Google Scholar 

  • Johnson P, Thieltges D (2010) Diversity, decoys and the dilution effect: How ecological communities affect disease risk. Journal of Experimental Biology 213:961–970

    Article  CAS  PubMed  Google Scholar 

  • Johnson PT, Preston DL, Hoverman JT, Richgels KL (2013) Biodiversity decreases disease through predictable changes in host community competence. Nature 494:230

    Article  ADS  CAS  PubMed  Google Scholar 

  • Johnson E, Sharma RSK, Cuenca PR, Byrne I, Salgado-Lynn M, Shahar ZS, Lin LC, Zulkifli N, Saidi NDM, Drakeley C (2022) Forest fragmentation drives zoonotic Malaria prevalence in non-human primate hosts. Biorxiv. 2:141

    Google Scholar 

  • Kettle C (2010) Ecological considerations for using dipterocarps for restoration of lowland rainforest in Southeast Asia. Biodiversity and Conservation 19:1137–1151

    Article  Google Scholar 

  • Kweka EJ, Zhou G, Gilbreath TM, Afrane Y, Nyindo M, Githeko AK, Yan G (2011) Predation efficiency of anopheles Gambiae larvae by aquatic predators in Western Kenya highlands. Parasites & Vectors 4:128–128

    Article  Google Scholar 

  • Laneng LA, Nakamura F, Tachiki Y, Vairappan CS (2021) Camera-Trapping Assessment of Terrestrial Mammals and Birds In Rehabilitated Forest in Inikea Project Area, Sabah, Malaysian Borneo. Landscape and Ecological Engineering 17:135–146

    Article  Google Scholar 

  • Lardizabal M, Hor C, Lee G, Bahudin N, Japir R, Fazrinah AD, Binti M, Chung A (2020) Comparison of Insect Assemblages (Butterfly, Dragonfly And Moth) in Different Lowland Forest Types in Sabah. Malaysia: Sepilok Bulletin, p 11

    Google Scholar 

  • Maharaj R (2003) Life table characteristics of anopheles Arabiensis (Diptera: Culicidae) under simulated seasonal conditions. Journal of Medical Entomology 40:737–742

    Article  CAS  PubMed  Google Scholar 

  • Mahmood F (1997) Life-table attributes of anopheles Albimanus (Wiedemann) under controlled laboratory conditions. Journal of Vector Ecology: Journal of the Society for Vector Ecology 22:103–108

    CAS  PubMed  Google Scholar 

  • Manin BO, Ferguson HM, Vythilingam I, Fornace K, William T, Torr SJ, Drakeley C, Chua TH (2016) investigating the contribution of peri-domestic transmission to risk of zoonotic Malaria infection in humans. Plos Neglected Tropical Diseases 10:E0005064

    Article  PubMed  PubMed Central  Google Scholar 

  • Melo FP, Arroyo-Rodríguez V, Fahrig L, Martínez-Ramos M, Tabarelli M (2013) On the hope for biodiversity-friendly tropical landscapes. Trends in Ecology & Evolution 28:462–468

    Article  Google Scholar 

  • Morand S, Jittapalapong S, Suputtamongkol Y, Abdullah MT, Huan TB (2014) Infectious diseases and their outbreaks in Asia-Pacific: Biodiversity and its regulation loss matter. Plos One 9:E90032

    Article  ADS  PubMed  PubMed Central  Google Scholar 

  • Morris EK, Caruso T, Buscot F, Fischer M, Hancock C, Maier TS, Meiners T, Müller C, Obermaier E, Prati D, Socher SA, Sonnemann I, Wäschke N, Wubet T, Wurst S, Rillig MC (2014) Choosing and using diversity indices: Insights for ecological applications from the german biodiversity exploratories. Ecology and Evolution 4:3514–3524

    Article  PubMed  PubMed Central  Google Scholar 

  • Nambiar E, Harwood C, Mendham D (2018) Paths To Sustainable wood supply to the pulp and paper industry in Indonesia after diseases have forced a change of species from Acacia to Eucalypts. Australian Forestry 81:148–161

    Article  Google Scholar 

  • Novianto D, Hadi U, Soviana S, Darusman H (2021) Species diversity and breeding site of mosquito Larvae (Diptera: Culicidae) in Macaca Fascicularis breeding area. IOP Conference Series: Earth and Environmental Science 2021:012039

    Google Scholar 

  • Patz JA, Daszak P, Tabor GM, Aguirre AA, Pearl M, Epstein J, Wolfe ND, Kilpatrick AM, Foufopoulos J, Molyneux D, Bradley DJ, Members Of The Working Group On Land Use Change Disease (2004) Unhealthy landscapes: Policy recommendations on land use change and infectious disease emergence. Environmental Health Perspectives 112:1092–1098

    Article  PubMed  PubMed Central  Google Scholar 

  • Payus C, Sentian J (2022) Satellite imagery system in Malaria transmission resulting from the land use/land cover change. Global Journal of Environmental Science and Management 8:545–560

    Google Scholar 

  • Phillips AJ, Simon C (1995) Simple, efficient, and nondestructive DNA extraction protocol for arthropods. Annals of the Entomological Society of America 88:281–283

    Article  CAS  Google Scholar 

  • Prist PR, Siliansky De Andreazzi C, Vidal MM, Zambrana-Torrelio C, Daszak P, Carvalho RL, Tambosi LR (2023) Promoting landscapes with a low zoonotic disease risk through forest restoration: The need for comprehensive guidelines. Journal of Applied Ecology 60:1510–1521

    Article  Google Scholar 

  • Putaporntip C, Kuamsab N, Seethamchai S, Pattanawong U, Rojrung R, Yanmanee S, Weng Cheng C, Jongwutiwes S (2022) Cryptic P. inui and plasmodium fieldi infections among symptomatic malaria patients in Thailand. Clinical Infectious Diseases 75:805–812

    Article  CAS  PubMed  Google Scholar 

  • Rattanarithikul, R., Harrison, B. A., Harbach, R. E., Panthusiri, P. & Coleman, R. E. 2006. Illustrated keys to the mosquitoes of Thailand Iv. Anopheles. The Southeast Asian Journal of Tropical Medicine and Public Health, 37(2).

  • Reid, J. 1968. Anopheline Mosquitoes of Malaya and Bornea. Anopheline Mosquitoes of Malaya and Bornea.

  • Reynolds G, Payne J, Sinun W, Mosigil G, Walsh RP (2011) Changes in forest land use and management in Sabah, Malaysian Borneo, 1990–2010, with a focus on the Danum valley region. Philosophical Transactions of the Royal Society b: Biological Sciences 366:3168–3176

    Article  Google Scholar 

  • Romell E, Hallsby G, Karlsson A, Garcia C (2008) Artificial canopy gaps in a Macaranga spp. dominated secondary tropical rain forest—effects on survival and above ground increment of four under-planted dipterocarp species. Forest Ecology and Management 255:1452–1460

    Article  Google Scholar 

  • Russell MC, Herzog CM, Gajewski Z, Ramsay C, El Moustaid F, Evans MV, Desai T, Gottdenker NL, Hermann SL, Power AG (2022) Both consumptive and non-consumptive effects of predators impact mosquito populations and have implications for disease transmission. Elife 11:E71503

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Saager E, Iwamura T, Jucker T, Murray K (2023) Deforestation for oil palm increases microclimate suitability for the development of the disease vector Aedes albopictus. Scientific Reports 13:9514

    Article  ADS  CAS  PubMed  PubMed Central  Google Scholar 

  • Sallum M, Peyton E, Wilkerson R (2005a) Six new species of the anopheles leucosphyrus group, Reinterpretation Of An. elegans and vector implications. Medical and Veterinary Entomology 19:158–199

    Article  CAS  PubMed  Google Scholar 

  • Sallum MAM, Peyton EL, Harrison BA, Wilkerson RC (2005b) Revision of the leucosphyrus group of anopheles (Cellia) (Diptera, Culicidae). Revista Brasileira De Entomologia 49:01–152

    Article  Google Scholar 

  • Sam J, Shamsusah NA, Ali AH, Hod R, Hassan MR, Agustar HK (2022) Prevalence of Simian Malaria among macaques in Malaysia (2000–2021): A systematic review. PlOS Neglected Tropical Diseases 16:E0010527

    Article  PubMed  PubMed Central  Google Scholar 

  • Saward-Arav D, Sadeh A, Mangel M, Templeton AR, Blaustein L (2016) Oviposition responses of two mosquito species to pool size and predator presence: Varying trade-offs between desiccation and predation risks. Israel Journal of Ecology & Evolution 62:143–148

    Article  Google Scholar 

  • Ser (2004) The Ser International Primer on Ecological Restoration. Tuscon Arizona: Society For Ecological Restoration International Science And Policy Working Group

    Google Scholar 

  • Singh B, Bobogare A, Cox-Singh J, Snounou G, Abdullah MS, Rahman HA (1999) A genus-and species-specific nested polymerase chain reaction malaria detection assay for epidemiologic studies. The American Journal of Tropical Medicine and Hygiene 60:687–692

    Article  CAS  PubMed  Google Scholar 

  • Singh B, Sung LK, Matusop A, Radhakrishnan A, Shamsul SSG, Cox-Singh J, Thomas A, Conway DJ (2004) A large focus of naturally acquired P. knowlesi infections in human beings. The Lancet 363:1017–1024

    Article  Google Scholar 

  • Speldewinde P, Slaney D, Weinstein P (2015) Is restoring an ecosystem good for your health? Science of the Total Environment 502:276–279

    Article  ADS  CAS  PubMed  Google Scholar 

  • St Laurent B, Burton TA, Zubaidah S, Miller HC, Asih PB, Baharuddin A, Kosasih S, Firman S, Hawley WA, Burkot TR (2017) Host attraction and biting behaviour of anopheles mosquitoes in South Halmahera, Indonesia. Malaria Journal 16:1–9

    Article  Google Scholar 

  • Tabarelli M, Lopes AV, Peres CA (2008) Edge-effects drive tropical forest fragments towards an early-successional system. Biotropica 40:657–661

    Article  Google Scholar 

  • Takano KT, Nakagawa M, Itioka T, Kishimoto-Yamada K, Yamashita S, Tanaka HO, Fukuda D, Nagamasu H, Ichikawa M, Kato Y, Momose K, Nakashizuka T, Sakai S (2014) The extent of biodiversity recovery during reforestation after swidden cultivation and the impacts of land-use changes on the biodiversity of a tropical rainforest region in Borneo. In: Sakai S, Umetsu C (eds) Social-Ecological Systems In Transition Tokyo: Springer Japan, pp 27–49. https://doi.org/10.1007/978-4-431-54910-9_2

    Chapter  Google Scholar 

  • Tan CH, Vythilingam I, Matusop A, Chan ST, Singh B (2008) Bionomics of anopheles Latens in Kapit, Sarawak, Malaysian borneo in relation to the transmission of zoonotic simian malaria parasite P. knowlesi. Malaria Journal 7:52

    Article  PubMed  PubMed Central  Google Scholar 

  • Thoradeniya T, Jayasinghe S (2021) Covid-19 and future pandemics: A global systems approach and relevance to sdgs. Globalization and Health 17:1–10

    Article  Google Scholar 

  • Van De Straat B, Sebayang B, Grigg MJ, Staunton K, Garjito TA, Vythilingam I, Russell TL, Burkot TR (2022) Zoonotic malaria transmission and land use change in Southeast Asia: What is known about the vectors. Malaria Journal 21:1–13

    Google Scholar 

  • Viani RA, Holl KD, Padovezi A, Strassburg BB, Farah FT, Garcia LC, Chaves RB, Rodrigues RR, Brancalion PH (2017) Protocol for monitoring tropical forest restoration: Perspectives from the atlantic forest restoration pact in Brazil. Tropical Conservation Science 10:1940082917697265

    Article  Google Scholar 

  • Viani RA, Barreto TE, Farah FT, Rodrigues RR, Brancalion PH (2018) Monitoring young tropical forest restoration sites: How much to measure? Tropical Conservation Science 11:1940082918780916

    Article  Google Scholar 

  • Vinogradov D, Sinev A, Tiunov A (2022) Predators as control agents of mosquito larvae in micro-reservoirs. Inland Water Biology 15:39–53

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Vythilingam I, Chan ST, Shanmugratnam C, Tanrang H, Chooi K (2005) The impact of development and Malaria control activities on its vectors in the Kinabatangan area of Sabah, East Malaysia. Acta Tropica 96:24–30

    Article  CAS  PubMed  Google Scholar 

  • Vythilingam I, Tan CH, Asmad M, Chan ST, Lee KS, Singh B (2006) Natural transmission of P. knowlesi to humans by anopheles latens in Sarawak, Malaysia. Transactions of the Royal Society of Tropical Medicine and Hygiene 100:1087–1088

    Article  CAS  PubMed  Google Scholar 

  • Vythilingam I, Wong ML, Wan-Yussof WS (2016) Current status of P. knowlesi vectors: A public health concern? Parasitology 145(1):32–40

    Article  PubMed  Google Scholar 

  • William T, Jelip J, Menon J, Anderios F, Mohammad R, Awang Mohammad TA, Grigg MJ, Yeo TW, Anstey NM, Barber BE (2014) Changing epidemiology of malaria in Sabah, Malaysia: Increasing incidence of P. knowlesi. Malaria Journal 13:390

    Article  PubMed  PubMed Central  Google Scholar 

  • Wong ML, Chua TH, Leong CS, Khaw LT, Fornace K, Wan-Sulaiman W-Y, William T, Drakeley C, Ferguson HM, Vythilingam I (2015a) Seasonal and spatial dynamics of the primary vector of P. knowlesi within a major transmission focus in Sabah. Malaysia. Plos Neglected Tropical Diseases 9:E0004135

    Article  PubMed  Google Scholar 

  • Wong ML, Vythilingam I, Leong CS, Khaw LT, Chua TH, Obrain B, Ferguson H, Drakely C (2015b) Incrimination of anopheles balabacensis as the vector for Simian Malaria in Kudat Division, Sabah, Malaysia. Journal of Microbiology, Immunology and Infection 48:S47–S48

    Article  Google Scholar 

  • Yang X, Bauhus J, Both S, Fang T, Härdtle W, Kröber W, Ma K, Nadrowski K, Pei K, Scherer-Lorenzen M (2013) Establishment success in a forest biodiversity and ecosystem functioning experiment in subtropical China (Bef-China). European Journal of Forest Research 132:593–606

    Article  Google Scholar 

  • Yap NJ, Hossain H, Nada-Raja T, Ngui R, Muslim A, Hoh B-P, Khaw LT, Kadir KA, Divis PCS, Vythilingam I (2021) Natural Human infections with P. cynomolgi, P. inui, and 4 other Simian Malaria Parasites, Malaysia. Emerging Infectious Diseases 27:2187–2191

    Article  PubMed  PubMed Central  Google Scholar 

  • Yayasan Sabah Group 2017. Conservation And Environmental Management

  • Yeong KL, Reynolds G, Hill JK (2016) Enrichment planting to improve habitat quality and conservation value of tropical rainforest fragments. Biodiversity and Conservation 25:957–973

    Article  Google Scholar 

  • Zhang C, Luo C, Yang R, Yang Y, Guo X, Deng Y, Zhou H, Zhang Y (2022) Morphological and molecular identification reveals a high diversity of anopheles species in the forest region of the Cambodia-Laos Border. Parasites & Vectors 15:1–17

    Article  CAS  Google Scholar 

Download references

Acknowledgements

With enormous gratitude, we would like to thank the field staff from the INIKEA project in Luasong, in particular the recently retired manager, David Alloysius for his patience and unwavering support over the years, and senior forest ranger Albert Lojingi, who oversaw and undertook the fieldwork during the district lockdowns In the Tawau district. Also, the tireless work of Benny Obrain ensured that the research was able to continue, albeit often sporadically, throughout the lockdown period. Benny Obrain collected the data from late 2019 through until mid-2021 and carried out mosquito identification and the PCR analysis. I’m extremely grateful for all his assistance, as well as the Universiti Malaysia Sabah for the use of their resources. Also, thanks must go to the Swedish Research Council and Ulrik Ilstedt at the Swedish University of Agricultural Science for continuing to provide funding for this ongoing research within the wider project ‘Balancing production and ecosystem services from degraded tropical rainforests to aid the transition to a more sustainable economy’. Finally, this research would not be possible without the support of the University of Western Australia, and my supervisors who each manage to offer unique and valuable guidance and assistance on this project.

Author information

Authors and Affiliations

  1. School of Agriculture and Environment, University of Western Australia, Albany, Australia

    Gael Davidson & Peter Speldewinde

  2. Borneo Medical and Health Research Centre (BMHRC), Universiti Malaysia Sabah, Kota Kinabalu, Malaysia

    Benny Obrain Manin

  3. School of Population and Global Health, University of Western Australia, Perth, Australia

    Gael Davidson & Angus Cook

  4. School of Biological Sciences, University of Adelaide, Adelaide, Australia

    Philip Weinstein

  5. Edulife Berhad, Kota Kinabalu, Sabah, Malaysia

    Tock H. Chua

Authors
  1. Gael Davidson
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Peter Speldewinde
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Benny Obrain Manin
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Angus Cook
    View author publications

    You can also search for this author in PubMed Google Scholar

  5. Philip Weinstein
    View author publications

    You can also search for this author in PubMed Google Scholar

  6. Tock H. Chua
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Tock H. Chua.

Ethics declarations

Conflict of interests

The authors declare there are no competing interests with this research.

Supplementary Information

Below is the link to the electronic supplementary material.

Supplementary file1 (DOCX 473 kb)

Rights and permissions

Springer Nature or its licensor (e.g. a society or other partner) holds exclusive rights to this article under a publishing agreement with the author(s) or other rightsholder(s); author self-archiving of the accepted manuscript version of this article is solely governed by the terms of such publishing agreement and applicable law.

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Davidson, G., Speldewinde, P., Manin, B.O. et al. Forest Restoration and the Zoonotic Vector Anopheles balabacensis in Sabah, Malaysia. EcoHealth (2024). https://doi.org/10.1007/s10393-024-01675-w

Download citation

  • Received:

  • Accepted:

  • Published:

  • DOI: https://doi.org/10.1007/s10393-024-01675-w

Keywords

Search

Navigation