Organic farming of maize crop enhances species evenness and diversity of hexapod predators

Abstract

Arthropod species diversity enhances ecosystem productivity and sustainability by increasing pollination and biological control services. Although, it is declining rapidly due to conventional agricultural intensification, organic agriculture with reduced reliance on agronomic inputs can regenerate ecosystems' resilience and restore them. Here, we report whether hexapod communities differ on both types of farming systems in small-scale field plot experiments, wherein Maize variety AG-589 was grown organically and conventionally in the 2020 and 2021 seasons. Livestock manure was applied in organic fields, whereas nitrogen and phosphorous were used as synthetic fertilizers in conventional fields. Hexapods were sampled three weeks after sowing once a week from the middle rows of subplots from both organically and conventionally grown maize. Twelve species of herbivores and four species of predators were recorded. Hexapod abundance overall and that of herbivores only was higher in conventionally cultivated maize, while predator abundance was higher in organic maize. Herbivores species diversity and evenness were significantly higher in conventional maize. Predator species diversity and evenness were significantly higher in organic maize fields. We noted predator abundance, diversity, and evenness as strong predictors to lower herbivore populations. These findings suggest that organic farming conserves natural enemies’ biodiversity and regulates herbivores with increased provision of suitable habitats and prey resources for natural enemies, leading to enhanced relative abundance in their specialized niches. Thus, organic agriculture can potentially mediate better ecosystem services.

Introduction

Global agriculture is now facing the unprecedented challenges of providing food, feed, and fiber for a rapidly growing population. Achieving these goals while maintaining ecosystem resilience, conserving biodiversity, and socio-economic balance of farmers represents a formidable challenge (Cooper & Dobson, 2007). Pesticides are often used to enhance agriculture production by suppressing agricultural pests, but the efficacy of pesticides is saturated over time (Lechenet et al., 2014; Gaba et al., 2016). Their repeated, long-term indiscriminate use can also degrade agricultural soils (Shahid et al., 2016) by affecting the physicochemical properties (AL-Ahmadi, 2019) as well as harming microbial communities and disturbing their beneficial activities (Arora et al., 2019). Biodiversity loss is another big challenge resulting from pesticide overuse (Maxwell et al., 2016). Biodiversity losses in terrestrial ecosystems also decrease provision of ecosystem services, like pollination and biomass production that provide vital benefits to humans and are important for ecosystem resilience (Tilman et al., 2002; Chaplin-Kramer et al., 2015). Yields of many crops are no longer increased in intensified farming (Ray et al., 2012), compromising the economic and environmental viability of this strategy (Tittonell, 2014).

Sustainable development aims at improving conservation, protection, restoration, and sustainability of the terrestrial ecosystems for the long-term benefits to mankind (Newbold et al., 2016). In order to maintain the balance between food security and conserving biodiversity, sustainable production practices like organic farming can lower ecological footprints without sacrificing the economic benefits and food security (Foley et al., 2011). Organic farming systems increase arthropod diversity and enhance ecosystem services, like predation and parasitism, ultimately reducing insecticide use by up to 97% (Mäder et al., 2002). Organic production maximizes the use of local resources to enhance soil fertility (Gomiero et al., 2011; Leifeld, 2012), but also has some socio-economic pros and cons for small holder farmers and developing countries. Since synthetic chemicals are prohibited in certified organic production systems, organic crops contain lower levels of insecticide and heavy metal residues compared to conventionally grown ones (Baker et al., 2002).

Herbivore densities in organic farms are generally regulated vertically and horizontally (fig. 1) i.e. mediated through bottom-up forces by soil or plant quality (Scherber et al., 2010; Letourneau et al., 2011), and top-down forces, those governed by the natural enemies (Cardinale et al., 2003; Finke & Denno, 2004) while horizontal herbivore regulation is through competition among members of same trophic levels. Organic farming may enhance below and above ground biodiversity and boost up plant resistance to herbivores, facilitating the bottom-up forces on the herbivores and possibly help to reduce insecticide loads and concerns in agriculture sector (Birkhofer et al., 2008; Krey et al., 2020; Gu et al., 2022). For instance, lower populations of leafhoppers, Circulifer tenellus (Baker) was noted in organic production systems of tomatoes due to higher accumulation of salicylic acid produced by well-established rhizosphere microbial communities (Blundell et al., 2020). So, organic farming can increase plant resistance and decrease plant attractiveness toward herbivores. Meanwhile, manure amended soil provides brown food web species to the generalist predators as alternate resources and directly support the top down effects in the organic farming (Brown and Tworkoski, 2004; Muñoz-Cárdenas et al., 2017). Organic farming enhances the abundance of arthropods (Tuck et al., 2014; Van Bruggen & Finckh, 2016), which, in turn, results in the higher resource competition among the members of same trophic levels (Kaplan & Denno, 2007). Altogether, organic farming is a system of sustainable production of crops that have the potential to regulate herbivore communities by supporting bottom up and top-down forces.

Figure 1. Horizontal and vertical modes of herbivorous pest regulation in organic farming.

Greater abundance and diversity (Gurr et al., 2003; Simon et al., 2011; Lichtenberg et al., 2017; Mabin et al., 2020) of arthropod predators translates to higher likelihood of biological control of herbivore on organic farms (Farooq et al., 2022). For example, increased predator diversity was observed to suppress cabbage aphid, Brevicoryne brassicae L. and green peach aphid Myzus persicae Sulzer (Hemiptera: Aphididae) populations in collards (Snyder et al., 2006). Herbivore suppression due to diverse predator communities might be linked with complementary use of shared prey resources (Niche complementarity hypothesis) (Straub & Snyder, 2006; Lynch et al., 2022). Moreover, soil organic matter improves soil microclimate in organic mix vegetables farms and is responsible for even distribution of coleopteran carabid predators (Aldebron et al., 2020). Crowder et al. (2010) also reported that more evenly structured and abundant predator communities can strongly suppress herbivore communities and increase plant growth in organic farms.

Although, a number of past studies have illustrated the role of organic farming in top-down regulation of herbivores by attracting insectivorous birds (Tremblay et al., 2001; Otieno et al., 2019a, 2019b), little has been reported on the community structure of hexapods, i.e., abundance, species evenness and diversity, in organic maize crops compared to conventional ones at field scales. Here, we aim to (1) assess the role of predator's abundance, diversity, and evenness in lowering the herbivore populations, and hypothesized that maize production systems (organic and conventional) affect (2) hexapod community structures and (3) their diversity.

Materials and methods

Field site description

We conducted experiments in the research area of Department of Entomology, Bahauddin Zakariya University (BZU), Multan, Pakistan, at an elevation of about 123 m above the sea level. The climatic conditions of the region is semi-arid with very hot summers (highest temperature 50°C) and cold winters (lowest temperature 4.5°C) with an average annual rainfall of 190 mm (Amer et al., 2009; Hussain et al., 2020). The Multan region produces major share of the country's staple food and fiber crops, such as wheat, maize, rice, and cotton. In the BZU, organic land has been maintained since 2003 for research purposes and livestock manure applied regularly to maintain soil fertility, whereas synthetic fertilizers have been used only in the conventional fields.

Experimental design

The seeds of maize variety AG-589 were cultivated on 10 August 2020, and 12 February 2021, in two separate maize experimental fields (organic and conventional). The organic and conventional fields were approximately1 km apart from each other. Each field comprised of three subplots, each measuring 20 × 6 m and separated from the nearby plot with one meter buffer zone which was a walking pathway without any vegetation. Although, individual subplots in either organic or conventional systems were very close to each other and were unlikely to be independent due to arthropod dispersal ability. Still, such dispersal was possible within the system but not between the systems (from organic to conventional fields) due to large separating difference between both systems. Additionally, to ensure effective sampling and to avoid edge effects, we counted hexapods from middle rows of individual subplots. We planted the seeds on the ridges (0.75 m apart) with the dibbling method at a plant spacing of 45 cm. One month prior to sowing, livestock manure (9.25 t ha⁻¹) with 0.46% Nitrogen (N), 0.46 mgg⁻¹ phosphorus (P) and 0.89 mgg⁻¹ potassium (Aziz et al., 2010) was applied into the organic field. We applied 227.24 kg ha⁻¹ and 143.26 kg ha⁻¹ N and P, respectively, as diammonium phosphate (18% N and 46% P) and urea (46% N), as per the local recommendation of the region after sowing of maize in the conventional field using the broadcast method. No pesticides were applied to either fields to suppress insect herbivores or weeds. Weeds were removed manually using hand.

Hexapod sampling

Hexapod populations were recorded from two consecutive years at weekly intervals. Sampling began three weeks after sowing, as negligible hexapods were present in the first two weeks, and remained continued once a week until crops were matured. Sampling was started from 2nd week of September in 2020 and 2nd week of March in 2021 that continued through 1st week of October in 2020 and 1st week of May in 2021. From each subplot of both field types (i.e., conventional and organic), we selected 16 plants at random from the middle two rows to avoid aggregation and edge effects and observed the whole plant to assess hexapod communities being present on selected plants. All hexapods were brought back to the laboratory and identified using morphological keys (Edde, 2021). The collected voucher specimens were stored as wet collection as well as dry collections in the IPM laboratory at Department of Entomology, Faculty of Agricultural Sciences and Technology, BZU, Multan, Pakistan. Hexapods were categorized as herbivores and predators based on their ecological role, feeding behavior, and trophic position. The phytophagous hexapods that feed on green plants and carnivore hexapods that feed upon phytophagous insects were classified as herbivores and predators, respectively. Hexapods were visually observed from the selected plants and the numbers of the larvae of Lepidoptera and Diptera, whereas adults and nymphs (for Hemiptera only) or larvae of Coleoptera, Thysanoptera, and Neuroptera (see Tables for species names) were counted and recorded.

Statistical analysis

We pooled the number of individuals for each insect species present in the organic and conventional maize fields across all sampling dates in each year. Principal component analysis (PCA) was used to measure various patterns of variations among the herbivore and natural enemy communities in organic and conventional maize production. For this purpose, two primary components were selected based on the eigenvalues as suggested by Kaiser (1974), who suggested that only those components will be selected that have eigenvalues greater than 1. Moreover, the first two components comprise the 90.99% proportion of variance. PCA analysis was performed using GraphPad Prism Version 9.0 (GraphPad Inc., San Diego, California, USA).

Diversity index of hexapods in organic and conventional fields was calculated by using the Shannon–Weaver diversity index formula (Shannon, 1948),

$$D = {\rm \;}-{\rm \Sigma }P_ilnP_i$$

where P_i represents the proportion of single species in the total abundance of a given sampling unit.

Dominance or evenness index of hexapods in organic and conventional fields was calculated by using the Simpson dominance index formula (Simpson, 1949),

$${\rm C} = {\rm \Sigma }( {P_i} ) ^2$$

where C is the Simpson dominance or evenness, P_i represents the proportion of single species in the total abundance of a given sampling unit.

The effect of farming systems on the overall abundance of hexapods and each functional group i.e., herbivores and predators, was assessed by using multivariate Analysis of Variance (MANOVA). The effect of farming system on individual species, diversity, and dominance were assessed by using non parametric generalized linear mixed model (GLMM). Year was fitted as the random effect in the models and the farming systems treated as the fixed effect. The relationship between herbivore density and four predictors i.e., predator density, predator diversity, and predator evenness was determined by using simple linear regression. The means of herbivore densities were tested for homogeneity of variance using a Shapiro–Wilk test and found to be typically non-normal. Therefore, these means were log (x + 1) transformed to satisfy conditions of normality and then subjected to analysis. All the data were analyzed by using Statistix 8.1 and graphs were plotted using Origin Pro 2022.

Results

Hexapod communities

A total of 16 hexapod species (12 herbivorous pest and 4 natural enemies) were recorded in this study from organic and conventional maize fields during 2020 and 2021 (Table 1). Figures 2 and 3 present hexapod abundance overall and that of herbivores and predators between conventional and organic maize. We found that overall hexapod abundance was higher in conventional fields (MANOVA: Wilks lambda = 0.327, F_{17, 174} = 21.1, P < 0.001); whereas herbivore density (MANOVA: Wilks lambda = 0.410, F_{13, 178} = 19.73, P < 0.001) was significantly lower in organic plots as compared to conventional maize plots. Conversely, predator density (MANOVA: Wilks lambda = 0.854, F_{4, 187} = 7.99, P < 0.001) was higher in organic vs conventional maize plots. Of all the hexapods observed, only populations of Rhopalosiphum maidis and Bemisia tabaci differed not significantly between organic and conventional maize plots (Table 2).

Figure 2. Effect of organic and conventional farming of maize on hexapod abundance (a), herbivores abundance (b) and predator abundance (c) in 2020 and 2021 pooled data. Bars and boxes topped with line having *, ** and *** show significant differences between groups at P < 0.05, 0.01, and 0.001, respectively.

Figure 3. Biplot of herbivores Atherigona soccata (As), Chilo partellus (Cp), Spodoptera litura (Sl), Spodoptera frugiperda (Sf), Helicoverpa armigera (Ha), Cicadulina mbila (Cm), Rhopalosiphum maidis (Rm), Bemisia tabaci (Bt), Frankliniella occidentalis (Fo), Oxycarenus hyalinipennis (Oh), Dalbulus maidis (Dm) and Chaetocnema pulicaria (Chap) and predators Chrysoperla carnea (Cc), Coccinella septempunctata (Cs), Chilomenes sexmaculata (Chs) and Brumoides suturalis (Bs). The light shaded spots represent the farming system i.e., organic and conventional, and arrows represent the vector of variables.

Table 1. Total numbers of hexapod species observed in organic and conventional maize fields

^a Only predacious phase (larvae) was observed.

Table 2. Generalized linear mixed model effects of organic and conventional farming of maize on seasonal totals (per plant) of herbivores and predators in 2020 and 2021 (insect counts pooled across the years)

^a Only predacious phase (larvae) was observed.

Farming systems and diversity indices

The Shannon–Weaver diversity index of overall hexapods were similar in both types of farming systems (F_{1, 4} = 3.44, P = 0.137, fig. 4a). Herbivores diversity was significantly lower in organic fields (F_{1, 4} = 262.81, P < 0.001, fig. 4b), while predator diversity was significantly higher in organic fields (F_{1, 4} = 256.82, P = 0.001, fig. 4c). Simpson dominance index of hexapods was significantly lower in organic maize when compared to conventional maize (F_{1, 4} = 158.01, P < 0.001, fig. 5a). Herbivore dominance was significantly lower in organic fields (F_{1, 4} = 78.61, P = 0.001, fig. 5b), while predator dominance was significantly higher in organic fields (F_{1, 4} = 335.7, P < 0.001, fig. 5c).

Figure 4. Shannon–Weaver diversity index for hexapods (a), herbivores (b), and predator (c) communities in organic and conventional maize in 2020 and 2021 (pooled data). Bars and boxes topped with line having ns show no significance and *** show significant differences between groups at P < 0.001.

Figure 5. Simpson dominance index for hexapods(a), herbivores (b), and predator (c) communities in organic and conventional maize in 2020 and 2021 (pooled data). Bars and boxes topped with line having *** show significant differences between groups at P < 0.001.

There was a significant, but negative relationship, between mean predator abundance and mean herbivore abundance (F _{1, 94} = 32.78, P < 0.001, fig. 6a). Predator diversity (F _{1, 4} = 101.29, P < 0.001, fig. 6b) and evenness (F _{1, 4} = 101.29, P < 0.001, fig. 6c) were significantly and negatively associated with herbivore abundance.

Figure 6. Relationships between the herbivore densities and (a) predator densities (b) predator diversity, and (c) predator evenness in maize fields. Note that population data for herbivore and predators are log (x + 1) transformed and pooled for both the years.

Discussion

We observed a higher abundance of herbivores in conventional maize plots, while predator abundance was greater in organic maize plots. In prior studies, hexapod herbivores of maize, including Ostrinia nubilalis Hubner (Phelan et al., 1995), often have ovipositional preference for conventionally grown maize compared to organic. Similarly, Aphis gossypii Glover was more abundant in conventional cotton fields, while its predators Coccinella septempunctata L. (Coleoptera: Coccinellidae), Chrysoperla carnea Stephens (Neuroptera: Chrysopidae) and Allograpta exotica (Widemann) (Syrphidae: Diptera) were in greater densities on organic cotton plants (Lu et al., 2015). Higher densities of cereal leaf beetles, Oulema spp. (Coleoptera, Chrysomelidae) and aphids were found in conventional wheat fields as compared to organic ones, whereas organic farming supported greater abundance of predators and parasitoids (Török et al., 2021). Another study demonstrated that phytophagous mites were significantly higher in conventional strawberry systems as compared to organic fields, whereas reverse situation was observed for hexapod natural enemies (Jacobsen et al., 2019). Conventional agricultural practices accompanied by the use of synthetic fertilizers enhance herbivore abundance (Yardım and Edwards, 2003). The manure application could reduce herbivore populations (Chau and Heong, 2005) by increasing predator densities in manure-treated areas (Brown and Tworkoski, 2004).

Our results show that organic maize supports a higher abundance of predators as compared to conventional maize. This direct positive impact of organic farming on predator abundance was consistent with previous studies, those demonstrating enhanced abundance of predator functional groups on organic fields (Bengtsson et al., 2005; Tuck et al., 2014). On organic farms, synthetic pesticides are rarely used to manage insect herbivores and farmland weeds (Muneret et al., 2019), which results in (1) increased availability of prey resources for predators and (2) increased local heterogeneity due to the production of natural vegetation in and around the field. Enhanced plant heterogeneity due to the production of natural vegetation in the form of farmland weeds is crucial for driving biological control on organic farms because they provide diverse floral resources and more hunting and hiding sites for predators (Galloway et al., 2021). Moreover, organic agriculture provides favorable microclimates responsible for enhanced plant resistance against herbivory supporting bottom up control of herbivores (Blundell et al., 2020) and also provide the brown food web species as an alternate host to the predators that directly triggers the top down control of herbivores (Muñoz-Cárdenas et al., 2017). Altogether, higher predator abundance can be attributed to favorable environments generated by organic managements like, lower pesticides exposure and supplement fields with offsite fertilizer like manure.

It has long been debated that increased predator biodiversity enhances biocontrol services in ecosystems (Root, 1973; Cardinale et al., 2003, 2006; Snyder et al., 2006; Farooq et al., 2022). Increasing the species evenness or enhancing the relative abundance of predators have the potential to improve biocontrol services (Crowder et al., 2010). The reason might be that relatively more even predator communities can occupy various complementary feeding niches. To sum up, more evenly distributed predator communities are potentially more important for providing biocontrol services on organic fields.

We noted predator abundance, diversity, and evenness as strong predictors of herbivore suppression because organic maize supports higher abundance of predators and there was a negative relationship between herbivore densities and predator abundance. This conclusion supports the natural enemy hypothesis that confers the herbivore suppression through enhanced abundance of natural enemies (Root, 1973; Cook-Patton et al., 2011). It is well documented that organic farming supports higher densities and diversity of predators (Muneret et al., 2019; Galloway et al., 2021). Increased abundance and evenness of predator species can improve or weaken the biological control (Hooper et al., 2005; Cardinale et al., 2006; Hillebrand et al., 2008; Crowder et al., 2010). The key factor determining the effect of predator evenness on herbivore suppression is the overlapped foraging areas of predator communities. If predator communities share common food niches and foraged in the overlapped areas of each other, they often encounter each other while searching and hunting for the same prey (Laubmeier et al., 2020). This phenomenon more likely results in negative interactions like interference and intraguild predation that ultimately reduce herbivore suppression.

Organic farming has socio-economics pros and cons for small land holders. The major concerns related to this production system in developing countries includes market barriers and certification (Gómez et al., 2011) of organic product, lower productivity (Connor, 2013; Ponisio et al., 2015) and lack of research and education for small scale farmers (Kleemann, 2011). Meanwhile, organic farming systems provide several benefits to small land holders. In spite of lower productivity of organic farms, the economic profitability of this system is still maximum as compared to others (Ramesh et al., 2010; Reganold and Wachter, 2016), because organic products are demanded globally and sold at a premium price as compared to conventional products (Aryal et al., 2009). In organic farming systems, substitutions of synthetic chemicals with low-energy and locally available farm inputs reduces the production cost of the farmer (Setboonsarng, 2006). However, this production system is labor intensive, but, the working of kith and kins on subsistence farms also reduces the external production costs of farmers (Kleemann, 2011). Organic farming has high environmental resilience to climatic shifts (Gattinger et al., 2012; Skinner et al., 2014), and together with the diversified ecosystem techniques (intercropping, crop rotation), it can potentially lower the risk of crop failure. Cost–benefit analysis of organic production systems proved reasonable benefits for resource-poor farmers due to the reduction of production costs in developing countries (Amoabeng et al., 2014). Nevertheless, organic farming is a favorable system for the subsistence growers as they do not need to buy synthetic chemicals like fertilizers and pesticides, rather they apply farmyard manure and extracts of plants or their parts as fertilizers and pesticides, respectively (Carvalho, 2017). Mostly, these inputs are easily and freely available in developing countries, for instance, manure of cattle raised for household needs can be used as organic fertilizers.

In conclusion, conventional maize supported a higher herbivore population, while organic maize supported a higher predator population. The predator diversity and evenness increased more in organic fields. We conclude that enhancing the relative abundance of predators has the potential to suppress herbivores on organic farms. Moreover, predator abundance, diversity, and evenness were shown to be strong predictors of herbivore suppression. To sum up, organic farming may not only be able to restore degraded ecological services but can also help subsistence farmers by lowering input costs for crop production. However, this is preliminary research and further research will be directed toward the determination of losses due to insect herbivores for cost–benefit analysis of both types of crops and evaluation of indigenous plant extracts for managing insect pests.