Birds and bats contribute to natural regulation of the millet head miner in tree-crop agroforestry systems

Highlights

• Vertebrates, including birds and bats, are effective predators of the millet head miner.

• They contribute to natural pest control and reduction of millet grain loss.

• The abundance of insectivorous birds is enhanced by tree diversity at a local scale.

• The contribution of trees for natural pest control is species-dependent. Trees can serve as refuges for pest (eg. baobab/moths) and predators (eg. palm tree/bats or neem/village weavers).

Abstract

A better understanding of environmental factors driving natural pest regulation is a major challenge for designing sustainable cropping systems. The objective of the present study was to assess the association between vegetation openness in traditional tree-crop agroforestry systems in Senegal, richness and abundance of vertebrates including insectivorous birds and bats, and their contribution to the natural regulation of crop pests. The millet head miner (MHM), Heliocheilus albipunctella (Lepidoptera, Noctuidae), a major constraint to increasing millet crop productivity in sub-Saharan Africa, was selected as a model system. Ten sites separated by at least one km from each other were selected in a 100 km² study area in the Peanut basin in Senegal. In each site, a pair of millet fields distant from at least 100 m each was selected according to a gradient of vegetation openness within a 100-m radius buffer with sampling plot (5 × 5 m) at the center. Nine insectivorous bird and bat species were recorded in millet fields over the 2017 cropping season and their predator status was confirmed by direct observation or DNA detection in fecal samples. Grain losses were reduced when panicles were accessible to birds and bats, confirming their net contribution to pest regulation. At a local scale, tree diversity and vegetation openness were important predictors of the abundance of insectivorous village weaver birds and grey-headed sparrows, respectively. Some tree species (soapberry trees and neems) indirectly contributed to natural regulation of the MHM likely by providing refuges to insectivorous vertebrates whereas other tree species (baobabs) provided disservices as possible refuges for the MHM moths. Further research is needed to better understand relationships between tree cover, food web interactions and natural pest suppression, so that specific conservation measures such as habitat management can be designed to improve pest control.

Introduction

During the last decades, worldwide losses of biodiversity have occurred at an unprecedented rate and agricultural intensification has been a major driver (Cardinale et al., 2012; Philpott et al., 2008; Tilman et al., 2002; Wilby and Thomas, 2002). The dramatic land use changes include the simplification of agricultural landscapes by deforestation and monoculture and the extensive use of agricultural inputs such as broad-spectrum insecticides to control crop pests, with detrimental impact on ecosystem health (Tscharntke et al., 2005; Barzman et al., 2015). Along with the loss of functional biodiversity, particularly biological control agents, such cultivated ecosystems have become more and more susceptible to pest outbreaks. This is particularly pregnant in southern contexts where arthropod pests pose a permanent threat to food security (Garrity et al., 2010). New models for crop protection are needed to reduce the dependence of agricultural systems on pesticides that stimulate ecological processes of natural regulation of crop pests (Brévault and Clouvel, 2019). One approach is to use the benefits of agroforestry systems to enhance or restore functional biodiversity (here, natural enemies of crop pests) to boost ecosystem services such as biological control of crop pests. A meta-analysis conducted by Pumariño et al. (2015) showed that agroforestry practices generally result in higher abundance of natural enemies of pests, lower pest abundance and less plant damage in perennial crops (e.g., coffee, cocoa and plantain) but not in annual crops (e.g., maize, rice and beans). However, studies carried out in Kenya showed that abundance of stem borers was significantly lower in Leucaena leucocephala (Lam.) (Fabales, Mimosaceae) alley cropping than in a maize monocrop (Ogol et al., 1999).

Among natural enemies of crop pests, vertebrates including insectivorous bats and birds can provide valuable ecosystem services such as suppression of insect pests (Maas et al., 2013; Maine and Boyles, 2015; Pejchar et al., 2018). By protecting crops through feeding on herbivorous pests, they can provide substantial increases in crop yields (Bael et al., 2008; Karp et al., 2013) and a true alternative to chemical insecticides (Bianchi et al., 2006). The abundance and diversity of semi-natural habitats within agricultural landscapes, particularly trees, has the potential to increase the abundance and diversity of birds and bats (Harvey et al., 2006; Redlich et al., 2018) and thus natural regulation of crop pests (e.g., nesting and breeding site, alternative preys). However, birds and bats can also negatively impact natural regulation of crop pests by consuming natural enemies of crop pests, i.e., intra-guild predation (Grass et al., 2017; Tschumi et al., 2018). On the other hand, trees can also benefit pests by providing food and refuges (Schroth et al., 2000). More research is thus needed on ecological issues to better understand how tree-crop agroforestry systems can contribute to enhance ecosystem services such as biological control of crop pests. Although a substantial body of research has been performed on the role of bats and birds in perennial cropping systems such as coffee plantations (Bael et al., 2008), few studies have focused on annual cropping systems as an unstable mosaic of habitats (Kennedy and Storer, 2000). More research is thus needed to deepen our knowledge of the life system of insectivorous birds and bats including seasonal population dynamics (e.g., breeding cycles, migration), multitrophic interactions within food webs (e.g. intraguild predation; see Grass et al., 2017), and temporal suitability of habitats in agricultural landscapes (Maas et al., 2016).

Agricultural landscapes in the “Peanut basin” in Senegal (West Africa) are generally structured by traditional agroforestry parkland systems (AFS), in which trees (mainly apple-ring acacias, Faidherbia albida) (Fabales, Fabaceae) are distributed in cultivated fields (Seyler, 1993). Even though the impact of those trees on soil fertility has been widely demonstrated, their effect on crop pests and biological control has been poorly studied (Hadgu et al., 2009; Umar et al., 2013). At the landscape scale, they offer a greater diversity of ecological niches in time and space than a simple mosaic of annual crops. The pearl millet, Pennisetum glaucum (L.) R. Br. (Cyperales, Poaceae), is the main annual crop in those agricultural systems. However, a key insect pest, the millet head miner (MHM) (Heliocheilus albipunctella de Joannis) (Lepidoptera, Noctuidae) is a permanent threat for increasing crop yields (Gahukar, 1984; Sow et al., 2018; Vercambre, 1978). Moths emerge from the soil one to two months after the beginning of the rainy season. After mating, females lay eggs in the millet panicle on the silk of the flower involucre or under stamens, but also on the floral peduncles or on the spine (Nwanze and Harris, 1992). The young larvae perforate the glumes and consume flowers, while the older ones cut off the floral peduncles (Gahukar, 1984; Vercambre, 1978), thus preventing grain formation. In the absence of any insecticide application by farmers, millet production relies on pest regulation by natural enemies (Bhatnagar, 1987; Nwanze and Sivakumar, 1990; Sow et al., 2019, 2017). A two-year monitoring of 90 millet fields and their surrounding landscape (2000 m-buffer around millet fields) showed that abundance of trees at the landscape scale significantly increased natural regulation of the MHM (Soti et al., 2019). Using high throughput molecular tools, the food web structures and ecological processes underlying natural regulation of crop pests by arthropods were documented and a large diversity of parasitoids and predators among arthropods were identified (Sow et al., 2018).

In the present study, we investigated the contribution of vertebrates, particularly insectivorous birds and bats, to the natural regulation of the MHM in tree-crop agroforestry systems in Senegal. We hypothesized that (i) abundance and diversity of trees at a local and landscape scale enhance the abundance and diversity of insectivorous birds, and that (ii) abundance and diversity of insectivorous birds at a local scale reduce pest incidence. We used satellite and drone imagery, remote sensing and geographical information system (GIS), to map and quantify the abundance and diversity of trees species at local and landscape scale around a set of 20 millet fields. Pest incidence and grain loss were evaluated by direct field observations on millet panicles while natural regulation was assessed using exclusion cages. In addition, the abundance and diversity of birds and bats was monitored in and around millet fields and fecal samples were collected to check for the presence of the MHM based on DNA analyses. Results are discussed in the light of relationships between tree diversity and abundance, role of vertebrates in food webs (ecosystem services vs. disservices) and biological control of crop pests for the deployment of ecologically-intensive cropping systems.