Continental-scale suppression of an invasive pest by a host-specific parasitoid underlines both environmental and economic benefits of arthropod biological control

Kris A G Wyckhuys; Prapit Wongtiem; Aunu Rauf; Anchana Thancharoen; George E Heimpel; Nhung T T Le; Muhammad Zainal Fanani; Geoff M Gurr; Jonathan G Lundgren; Dharani D Burra; Leo K Palao; Glenn Hyman; Ignazio Graziosi; Vi X Le; Matthew J W Cock; Teja Tscharntke; Steve D Wratten; Liem V Nguyen; Minsheng You; Yanhui Lu; Johannes W Ketelaar; Georg Goergen; Peter Neuenschwander

doi:10.7717/peerj.5796

Continental-scale suppression of an invasive pest by a host-specific parasitoid underlines both environmental and economic benefits of arthropod biological control

PeerJ. 2018 Oct 19:6:e5796. doi: 10.7717/peerj.5796. eCollection 2018.

Authors

Kris A G Wyckhuys^{1

2

3

4

5}, Prapit Wongtiem⁶, Aunu Rauf⁷, Anchana Thancharoen⁸, George E Heimpel⁹, Nhung T T Le¹⁰, Muhammad Zainal Fanani⁷, Geoff M Gurr^{1

11}, Jonathan G Lundgren¹², Dharani D Burra¹³, Leo K Palao¹³, Glenn Hyman¹⁴, Ignazio Graziosi^{15

16}, Vi X Le¹⁰, Matthew J W Cock¹⁷, Teja Tscharntke¹⁸, Steve D Wratten^{1

19}, Liem V Nguyen¹⁰, Minsheng You¹, Yanhui Lu⁵, Johannes W Ketelaar²⁰, Georg Goergen²¹, Peter Neuenschwander²¹

Affiliations

¹ Institute of Applied Ecology, Fujian Agriculture & Forestry University, Fuzhou, Fujian, China.
² School of Biological Sciences, University of Queensland, Brisbane, Australia.
³ Institute of Insect Sciences, Zhejiang University, Hangzhou, China.
⁴ CGIAR Program on Roots, Tubers and Banana, International Center for Tropical Agriculture, Hanoi, Vietnam.
⁵ Institute of Plant Protection, China Academy of Agricultural Sciences, Beijing, China.
⁶ Rayong Field Crops Research Center, Thai Department of Agriculture, Rayong, Thailand.
⁷ Bogor Agricultural University, Bogor, Indonesia.
⁸ Kasetsart University, Bangkok, Thailand.
⁹ University of Minnesota, Minneapolis, United States of America.
¹⁰ Plant Protection Research Institute, Hanoi, Vietnam.
¹¹ Charles Sturt University, Orange, Australia.
¹² Ecdysis Foundation, Estelline, United States of America.
¹³ International Center for Tropical Agriculture CIAT, Hanoi, Vietnam.
¹⁴ International Center for Tropical Agriculture CIAT, Cali, Colombia.
¹⁵ University of Kentucky, Lexington, United States of America.
¹⁶ World Agroforestry Center ICRAF, Nairobi, Kenya.
¹⁷ CABI, Wallingford, United Kingdom.
¹⁸ University of Goettingen, Goettingen, Germany.
¹⁹ Lincoln University, Christchurch, New Zealand.
²⁰ Food and Agriculture Organization, Bangkok, Thailand.
²¹ International Institute of Tropical Agriculture, Cotonou, Benin.

Abstract

Biological control, a globally-important ecosystem service, can provide long-term and broad-scale suppression of invasive pests, weeds and pathogens in natural, urban and agricultural environments. Following (few) historic cases that led to sizeable environmental up-sets, the discipline of arthropod biological control has-over the past decades-evolved and matured. Now, by deliberately taking into account the ecological risks associated with the planned introduction of insect natural enemies, immense environmental and societal benefits can be gained. In this study, we document and analyze a successful case of biological control against the cassava mealybug, Phenacoccus manihoti (Hemiptera: Pseudococcidae) which invaded Southeast Asia in 2008, where it caused substantial crop losses and triggered two- to three-fold surges in agricultural commodity prices. In 2009, the host-specific parasitoid Anagyrus lopezi (Hymenoptera: Encyrtidae) was released in Thailand and subsequently introduced into neighboring Asian countries. Drawing upon continental-scale insect surveys, multi-year population studies and (field-level) experimental assays, we show how A. lopezi attained intermediate to high parasitism rates across diverse agro-ecological contexts. Driving mealybug populations below non-damaging levels over a broad geographical area, A. lopezi allowed yield recoveries up to 10.0 t/ha and provided biological control services worth several hundred dollars per ha (at local farm-gate prices) in Asia's four-million ha cassava crop. Our work provides lessons to invasion science and crop protection worldwide. Furthermore, it accentuates the importance of scientifically-guided biological control for insect pest management, and highlights its potentially large socio-economic benefits to agricultural sustainability in the face of a debilitating invasive pest. In times of unrelenting insect invasions, surging pesticide use and accelerating biodiversity loss across the globe, this study demonstrates how biological control-as a pure public good endeavor-constitutes a powerful, cost-effective and environmentally-responsible solution for invasive species mitigation.

Keywords: Ecological intensification; Ecological safety; Ecosystem services; Insect biological control; Insect parasitism; Invasion biology; Sustainable agriculture; Tropical agro-ecosystems.

Grants and funding

This initiative was conducted as part of an EC-funded, IFAD-managed, CIAT-executed programme (CIAT-EGC-60-1000004285), while additional funding was provided through the CGIAR-wide Research Program on Roots, Tubers and Banana (CRP-RTB). Activities in Thailand and Indonesia during 2017 were finalized using own resources of Kris AG Wyckhuys. There was no additional external funding received for this study. The funders had no role in study design, data collection and analysis, decision to publish, or preparation of the manuscript.