Unsung heroes: fixing multifaceted sustainability challenges through insect biological control
Introduction
Insect biodiversity underpins sustainable food systems and secures a delivery of myriad ecosystem services such as pollination, nutrient cycling or biological pest control [1,2••]. In conventional agro-production systems, as typified by genetically uniform monocultures, ‘locked-in’ chemical dependencies and heavy mechanization, these biodiversity-based ecosystem services have steadily degraded [3, 4, 5]. Amongst others, a unidimensional focus on yield gain has deepened farmers’ perceived need for petroleum-derived inputs, while downplaying the role of ecosystem service-providing organisms such as beneficial insects. This is further aggravated by scant, empirically derived information on insects’ contribution to ecosystem service delivery in agricultural settings [6]. Parallel to those trends, the unrelenting appearance of new invasive pests puts mounting pressure on agro-ecosystems, negatively impacting biodiversity, ecosystem functioning and primary productivity while often triggering environmentally disruptive responses.
Not only are the monetary impacts of invasive species infrequently assessed [7], there also is a deficient understanding of how they affect sustainability currencies for example, environmental integrity or societal wellbeing. A failure to conduct these assessments in an unbiased, comprehensive fashion can obscure biodiversity-driven mitigation measures [8,9] and ultimately favor unsuitable practices [10•]. In light of the above, today’s entomologists need to examine the multi-faceted benefits of biodiversity-mediated tools for invasive species mitigation. Doing so in the tropics is particularly rewarding, as this part of the world is bound to bear the brunt of global environmental change and its highly biodiverse ecosystems tend to be managed by some of the world’s poorest and most vulnerable people [7,11].
Insect biological control (BC) entails the scientifically guided conservation, augmentation or introduction of beneficial organisms for the management of (either native or invasive) crop pests, pathogens or weeds [12,13]. The judicious selection and ensuing release of non-native species for the mitigation of invasive pests (so-called ‘classical biological control’) has a long and rich history typified by hundreds of success stories [14]. Though few ill-advised interventions in the mid-1900s did result in unintended ecological impacts [15], modern-day biological control has become a desirable, environmentally sound and near ‘tailor-made’ approach for invasive pest control. One widely acclaimed BC endeavor is the 1980’s campaign against the invasive mealybug Phenacoccus manihoti (Hemiptera: Pseudococcidae) on African cassava Manihot esculenta (Malpighiales: Euphorbiaceae), using the neotropical parasitoid Anagyrus lopezi (Hymenoptera: Encyrtidae) [16]. Through an internationally coordinated initiative by the Consultative Group of International Agricultural Research (CGIAR) and Centre for Agriculture and Bioscience International (CABI), this host-specific wasp was collected in Paraguay by the late Anthony C. Bellotti, screened under quarantine conditions in the UK and released in western Africa during the early 1980s. Laboratory rearing, field testing and follow-up introductions over 1981–1995 permitted the establishment of A. lopezi in 26 African countries, causing substantial reductions in P. manihoti population levels and securing a near-total recovery of local crop yields.
In 2008, P. manihoti made its accidental arrival in Southeast Asia (Figure 1), threatening the viability of a thriving cassava industry and prompting an internationally endorsed, preventative use of neonicotinoid insecticides over extensive areas. Yet, in 2009, Thailand’s Royal Government equally opted to mobilize A. lopezi. From 2010 onward, parasitoids were mass-reared and released across Southeast Asia, successfully established at a regional level and suppressed invasive P. manihoti populations [17]. Attaining average parasitism levels of 30.0 ± 24.0% (n = 110), A. lopezi amply surpassed established thresholds for successful biological control, drove down mealybug numbers and restored crop yields [17]. Though most local farmers remained unaware of the exact identity, ecology and dispersal mode of either crop antagonist or beneficial [18], BC provided a cost-free, self-propelling means of pest suppression for millions of Asian smallholder families. Here, we illuminate several important yet rarely quantified outcomes of this successful case of biological control and frame them within the broader context of the United Nations Sustainable Development Goals (UN-SDG) (Figure 2).
Section snippets
A ‘gushing well’ of benefits
As a climate-hardy tropical root crop, cassava (Manihot esculenta) is a prime food, feed, fiber and bio-energy crop cultivated on ∼25 million ha worldwide. In Southeast Asia alone, cassava cropping sustains the livelihoods of millions of smallholder farmers and constitutes a dependable source of rural income. While P. manihoti resulted in up to 84% yield drops in Africa and often led to total crop loss [16], those pest-induced impacts were restored through one-time releases of A. lopezi in the
SDG 1 – no poverty
In Southeast Asia, mealybug biological control enabled a (lasting) yield recovery of 5.3–10.0 tonnes/ha for two popular cassava varieties [17]. Farm-gate benefits ranged between US $515−938 per ha in Thailand and $1,500-$2,750 in Indonesia, when considering a mealybug-induced yield loss of 72.9% (i.e. ‘worst case’) or a 40% conservative scenario (Table 1). While insecticide-based management of invasive pests comes with a non-negligible cost (e.g. US$ 1.3–2.3 billion/year for global mitigation of
SDG 8 – decent work and economic growth
By reconstituting crop yields, millimeter-long wasps plausibly freed capital to upgrade farm equipment, acquire inputs and spur agricultural productivity growth (while also stimulating local cassava processing, starch extraction and related services). Given the substantial household-level savings emanating from mealybug BC, incremental spending on non-farm goods and services is expected to feed forward into the domestic economy [23]. Particularly in low-input smallholder systems, this consumer
SDG 14 - life on land
Industrialized agriculture and invasive species are major drivers of biodiversity loss, and the prevailing ‘produce-at-all-costs’ approach to farming has resulted in rising levels of chemical contaminants and greenhouse gas (GHG) emissions [4,33]. With a near-flawless record of ecological safety [34], insect BC is a powerful tool for the preservation and restoration of natural ecosystems [35]. Within agricultural settings, BC not only enhances resource use efficiencies or defuses a need for
SDG 2 - zero hunger
Cassava is a prime source of carbohydrates for millions of people and its nutrient-dense roots are a valued staple food – particularly in Africa. In a similar way as the blight fungus Phytophtora infestans triggered the 1845 Irish potato famine, P. manihoti compromised food security and instigated famine among cassava-reliant livelihoods in sub-Saharan Africa during the 1970s-80 s. More specifically, P. manihoti resulted in a decline of birth rate (−5.8%) or fertility rate (−5.5%) along its
SDG 3 - good health and wellbeing
In Asia’s cassava crop, BC defused a need for insecticide dips and thus lowered farmers’ exposure to hazardous chemicals. In other pest-crop systems, on-farm use of biological control against endemic or invasive pests can also benefit consumers — delivering similarly nutritious foods with less (or no) pesticide residues as compared to conventional pest management regimes [45]. These biodiversity-centered approaches further enhance resistance to food-borne human pathogens and have multiple
Concluding remarks
Through modern times, insects have found themselves uncomfortably associated with doom-laden terms - either as harbingers of disaster or as ‘canaries-in-the-coalmine’ signaling ecosystem collapse. For centuries, insect herbivores and disease vectors have been depicted as horsemen of the Apocalypse, sowing pestilence, famine and death [49]. While crop-feeding insects possibly raise the Malthusian specter for ecologically brittle farming systems or food-deficit environments in a rapidly warming
Conflict of interest statement
Nothing declared.
References and recommended reading
Papers of particular interest, published within the period of review, have been highlighted as:
• of special interest
•• of outstanding interest
Acknowledgements
We are grateful to Bernardo Creamer for providing valuable comments and suggestions on the economic impact assessment. The development of this manuscript did not receive any specific grant from funding agencies in the public, commercial, or not-for-profit sectors.
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