Elsevier

Biological Control

Volume 121, June 2018, Pages 129-139
Biological Control

Landscape context does not constrain biological control of Phenacoccus manihoti in intensified cassava systems of southern Vietnam

https://doi.org/10.1016/j.biocontrol.2018.02.011Get rights and content

Highlights

  • Asia’s cassava mealybug populations are suppressed following A. lopezi introduction.

  • Mealybug incidence, but not abundance, is highest in high-diversity settings.

  • Parasitism is unaffected by landscape context.

  • Hyperparasitism is enhanced in diverse settings at particular crop age.

  • Parasitoid density dependency is more pronounced in low-diversity settings.

Abstract

In 2008, the cassava mealybug, Phenacoccus manihoti (Homoptera: Pseudococcidae) was inadvertently introduced to Southeast (SE) Asia, where it inflicted severe damage on cassava crops, and impacted countless farming families and rural agro-industries. The host-specific endophagous parasitoid Anagyrus lopezi (Hymenoptera: Encyrtidae) was imported into Thailand in 2009, and subsequently released in neighboring countries. At present, nothing is known about the degree to which A. lopezi establishment, in-field colonization and impact on P. manihoti populations is shaped by local agro-landscape context. In this study, we contrasted temporal population fluctuations of P. manihoti, A. lopezi, and associated hyperparasitoids within low- and high-diversity landscapes in Tay Ninh (Vietnam). Across years and landscape types we found 24.8 ± 17.7% (mean ± SD) plants infected with P. manihoti and on average 5.6 ± 5.3 mealybugs per cassava tip. High parasitism levels were attained across both years, with season-long averages of 49.9–52.1% in either low- or high-diversity settings. Hyperparasitism levels were on average 2.8 ± 5.4%, and a total of three hyperparasitoid species were recorded. Cassava age was a significant predictor of P. manihoti incidence, abundance, parasitism rate and hyperparasitism rate. Landscape type significantly affected P. manihoti incidence and hyperparasitism rate (at particular ages), but not P. manihoti abundance or parasitism rate. At the scale of individual cassava tips and entire fields, A. lopezi exhibited a strong density-dependent response to P. manihoti during the early season. This work constitutes the first, comprehensive assessment of A. lopezi establishment, parasitism rates, and parasitoid x host dynamics from a key cassava-growing region in SE Asia. Our study underlines how this exotic parasitic wasp effectively suppresses a globally-important insect pest in its newly invaded range, thus providing cost-free, environmentally-sound and lasting control across the developing-world tropics.

Introduction

The cassava mealybug, Phenacoccus manihoti Matile-Ferrero (Homoptera: Pseudococcidae) is a prominent pest of cassava (Manihot esculenta Crantz; Euphorbiaceae) and one of the world’s most notorious invasive species. Endemic to the Paraguay River basin, P. manihoti was inadvertently introduced into Africa during the early 1970s and subsequently spread through the continent’s extensive cassava belt (Herren and Neuenschwander, 1991, Bellotti et al., 2012). Capable of inflicting yield losses up to 58–84% (Nwanze, 1982, Schulthess et al., 1991), P. manihoti devastated local cassava production and impacted food security for underprivileged rural populations across sub-Saharan Africa. In late 2008, this same pest was detected in Thailand, where it was reportedly causing root yield reductions up to 50% and economic losses over US $30 million nationally (Muniappan et al., 2009, TTTA, 2011). By 2014, P. manihoti had spread extensively into neighboring countries and several Indonesian islands (Sartiami et al., 2015, Graziosi et al., 2016). Climate-based niche modeling further revealed that other key production areas in eastern Indonesia and the Philippines are also climatically suitable for P. manihoti (Yonow et al., 2017). As Southeast Asia houses a multi-billion dollar cassava industry and accounts for nearly 95% of the world’s cassava exports (Cramb et al., 2017), the (socio-)economic impacts of this pest were projected to be exceptionally large.

With the 1981 introduction of Anagyrus lopezi (De Santis) (Hymenoptera: Encyrtidae) in West Africa, a globally-acclaimed biological control program against P. manihoti was started (Neuenschwander, 2001). This solitary, host-specific parasitoid had earlier been collected in Paraguay and southern Brazil from small P. manihoti colonies on cassava (Lohr et al., 1990). Following its release in Nigeria, A. lopezi promptly established and suppressed P. manihoti population levels from more than 100 to fewer than 10–20 individuals per tip (Hammond et al., 1987). In less than three years following its release, A. lopezi had effectively dispersed over 200,000 km2 and colonized the vast majority of cassava fields within this range (Herren et al., 1987). Though multiple endemic primary parasitoids and hyper-parasitoids were recorded in mealybug-invaded areas in Africa (Neuenschwander et al., 1987, Neuenschwander and Hammond, 1988), these largely did not impede the success of A. lopezi as biological control agent (Neuenschwander, 2001). Overall, the parasitic wasp successfully established in 26 different African countries, prevented wide-spread famine and generated long-term economic benefits of US$ 9.4-20.2 billion (Zeddies et al., 2001).

In late 2009, A. lopezi was introduced from West Africa into Thailand and subsequently into Indonesia, through a joint endeavor between the Food and Agriculture Organization (FAO), CGIAR centers and Thai governmental institutions (Winotai et al., 2010, Wyckhuys et al., 2015). Other methods promoted for P. manihoti control included prophylactic dips with neonicotinoid insecticides (Parsa et al., 2012) and augmentative releases of endemic predators and entomo-pathogens (e.g., Saengyot and Burikam, 2012, Sattayawong et al., 2016). However, it has largely been deemed that A. lopezi effectively suppressed local mealybug populations. In a first regional assessment during 2014–2015, A. lopezi was routinely found in P. manihoti-affected fields at parasitism levels of 10–57% (Wyckhuys et al., 2017a). Yet, from smallholder fields in Cambodia, a diverse and speciose complex of hyperparasitoids or mummy parasitoids was equally recorded (Wyckhuys et al., 2017b).

Natural enemy abundance and performance, as much as pest pressure, are shaped by a wide range of variables at a field, farm, and agro-landscape level. In Asian cassava fields, patch-level characteristics, such as soil parameters and a plant’s phytopathogen infection status, readily modulate A. lopezi × P. manihoti interactions (Wyckhuys et al., 2017a, Wyckhuys et al., 2017b). Landscape-dependent impacts on cassava mealybug biological control have rarely been inferred in past studies, and so far have not been studied in-depth. Though the effects of landscape structure on natural enemy abundance, diversity, and activity have been relatively well investigated (e.g., Bianchi et al., 2006, Chaplin-Kramer et al., 2011, Veres et al., 2013, Schellhorn et al., 2015b), much less is known about its impacts on pest pressure or (natural) biological control. Yet, for specialist parasitoids such as A. lopezi, habitat loss and landscape simplification could be particularly disruptive (Cagnolo et al., 2009). Also, while landscape-level interactions have been assessed to a fair extent for annual cropping systems under temperate conditions, they have only received scant attention in (semi-)perennial cropping systems in the tropics (but see Tylianakis et al., 2007, Pak et al., 2015). Lastly, fourth-trophic level organisms, such as hyperparasitoids, have only received peripheral attention in landscape ecology studies (Rand et al., 2012, Plećaš et al., 2014), even though they are highly responsive to landscape complexity, are connected to arthropod population dynamics across habitats, and may release herbivores, such as P. manihoti, from biological control (Sullivan and Volkl, 1999).

In this study, we examine landscape-level effects on P. manihoti biological control in intensified cassava cropping systems of southern Vietnam (i.e., Tay Ninh province). We characterize overall P. manihoti population levels across two successive growing seasons, assess A. lopezi establishment and impact, and describe the resident hyperparasitoid community. Furthermore, we contrast mealybug-parasitoid-hyperparasitoid dynamics in fields embedded within simplified, large-scale landscapes vs. complex, small-scale settings. This study adopts a landscape ecology approach, yet is no landscape analysis sensu stricto as it is not guided by structural indicators of landscape composition or spatial configuration (Mühlner et al., 2010, Birkhofer et al., 2018). Our work constitutes the first, comprehensive assessment of A. lopezi parasitism rates and parasitoid × host dynamics from a key cassava-growing area in SE Asia, examines P. manihoti biological control through a (novel) landscape ecology lens, and provides valuable insights to guide further (invasive) pest mitigation programs.

Section snippets

Study sites

Our study was conducted in several rural communes of Tay Ninh province, southern Vietnam (Fig. 1); an area characterized by highly-intensified cassava production, with staggered (overlapping) planting and near-continuous, year-long cultivation. Local cassava fields are routinely established with locally-sourced stem cuttings (i.e., stakes), receive ample fertilizer and herbicide inputs during the first 3–4 months, and are manually harvested at 9–12 months after planting. Overall, two different

Mealybug & parasitoid community composition

In field surveys from 2014 to 2015, a total of four different mealybug species were recorded from cassava fields: P. manihoti, Pseudococcus jackbeardsleyi Gimpel and Miller, Paracoccus marginatus Williams and Granara de Willink, and Ferrisia virgata (Cockerell). Across sites and years, P. manihoti constituted 91.4% of the mealybug complex, with other species representing 5.7%, 2.8% and 0.2%, respectively. Field-level incidence of P. manihoti ranged from 0% to 82% across both years, with an

Discussion

As the stage for one of the world’s greatest biological control successes (Neuenschwander, 2001), cassava cropping systems possess unique and noteworthy features. Being long-season crops exposed to comparatively few disturbances, cassava systems provide habitats of prolonged durational stability and vegetational complexity for myriad natural enemies. The secretion of extra-floral nectar by the cassava plant also constitutes a favorable trait for multiple beneficial organisms, including

Acknowledgments

This manuscript presents original datasets that result from collaborative research, with trials jointly conceptualized, defined and executed by Vietnamese counterparts, CIAT personnel and international cooperators. We would like to thank Drs. Nguyen Van Liem, Trinh Xuan Hoat and Le Xuan Vi at Vietnam’s Plant Protection Research Institute (PPRI-VAAS), for their support to field staff and for facilitating this 2-year insect survey. We are grateful to collaborators from Hung Loc Research station

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