Natural Enemies and Pest Control in Field-Grown Crop in Southern Senegal

Crop pests are a permanent threat to horticultural production. Several control methods are recommended for their control, including biological control. This method based on the use of natural enemies is not well established. The objective of this study was to assess the diversity and abundance of natural enemies of crop pests. A survey of crops associated with pests was carried out on 144 fields in southern Senegal to measure the diversity and abundance of natural enemies of various crop pests, determine the native parasitoid complex and assess parasitism rates. Ecological indices were calculated to assess the diversity of natural enemies. A total of 25 natural enemy species were identified, including 15 parasitoids and 10 predators. Predatory Hemiptera and Parasitoid Hymenoptera were high biodiversity. The parasitism rates vary between 0 and 50% depending on the abundance of pests and parasitoid species. Knowledge of the diversity of natural enemies and the understanding of trophic interactions with pests are important in the development of biological crop protection in order to preserve resilience in agroecosystems.


Introduction
In Senegal, market gardening is mainly developed in the Niayes agro-ecological zone where pests cause a significant loss of crops [1] [2]. In Senegal's agro-ecological zones, vegetable production is subject to various constraints, including the pressure of insect pests. These pests are a permanent threat to horticultural production. The use of natural enemies such as predators or parasitoids for pest control is more economically viable and environmentally safer than currently recommended synthetic insecticides. Chemical control is the main strategy used to control pests as consequence of the role of natural enemies in the biological control of pests is very poorly understood by vegetable farmers in Senegal. Indeed, chemical control causes environmental pollution [3] and pesticide resistance to insects [4]. Chemical control contributes significantly to the loss of ecosystem services such as biological pest control and favours pest damage to crops. Biological control aims to keep pest populations low through natural enemies in order to restore ecosystem services and build resilience in agro-ecosystems. Natural enemies are considered to be important in agricultural ecosystems [5]. However, biological control service provided by natural enemies sometimes was very poorly known by farmers in Senegal. This method aims to enhance pest control in the field [6].
Native natural enemies regulate pest populations through predation or parasitism [7]. In Casamance, the implementation of numerous agricultural programs and projects has favoured the development of new market garden production areas which contribute to economic development and the fight against unemployment [8]. Pests are a constraint in these vegetable production basins because few research studies have been carried out on the natural enemies. The objective of this study is to assess the species richness and abundance of natural enemies of pests associated with vegetable crops.

Study Area
This study was conducted in three localities in the southern region of Senegal from May 2017 to June 2019 ( Figure 1). The localities surveyed were Bignona, Oussouye, and Ziguinchor. These three departments represent together the region of Ziguinchor known as "Basse Casamance". The climate in this area is sub-Guinean and is characterized by one rainy season (June-October) and one dry season (November-May). These localities were randomly selected among others based on the crop present in the area (Figure 1). "Basse Casamance" region is located at 12˚33' North latitude and 16˚16' West longitude, magnetic declination 13˚05.
Its altitude is 19.30 m in the southwestern part of Senegal. It covers an area of 7.339 km 2 or 3.73% of the national territory [9].

Sample Processing and Identification of Natural Enemies
The inventory of natural enemies of pests associated with crops was carried out at the vegetable fields of the agricultural holdings. Overall, 144 crop fields were surveyed in three localities. In each locality, 48 fields were visited. The surveys of the vegetable fields were carried out each week during their availability period.
Predators were captured using a mouth-suction aspirator or a flexible forceps.  Predators are placed in a plastic jar containing absorbent paper and ethyl acetate in order to kill them and to facilitate conservation and identification. The collected samples are kept in tubes containing 70% alcohol for identification. The larvae of pests were collected and monitored in the laboratory. They were fed with fresh leaves from their host plants, which were renewed every day. The parasitoids were obtained after their emergence on the larvae monitored. For identification, the insects were observed with the "Dinolite" magnifying glass version

Assessment of Natural Enemy Diversity
Ecological indices have been used to assess the diversity of natural enemies associated with crop pests. Statistical analyses were performed using PAST software,

Results
Natural enemies' species are classified according to their functional groups (predators and parasitoids). Ecological indices were used to assess the diversity of natural enemies associated with pests

Evaluation of the Diversity of Natural Enemies of Pests
Natural enemies were associated with pests. In order to evaluate these natural enemies, the diversity and abundance of pests were shown according to localities ( Table   1). Abundance of pests and the number of host plants found are more important in Ziguinchor than in Bignona and Oussouye. On the other hand, the number of pest species is lower in Oussouye followed by Ziguinchor and Oussouye Identification of the main groups of natural enemies is carried out to show their trophic relationships with the pests to understand interactions between diversity at different trophic levels.
Pest associated with host plants were more abundant in the locality of Ziguinchor compared to the other two localities (χ 2 =1226.843, df = 2, p < 0.0001) ( Figure 2).
The locality of Oussouye, which has the greatest biodiversity, has a lower abundance of pest associated with host plants.

Predators diversity
Pests attacked by predators are identified to show the number of target or prey  pest species. A total of 10 predator species belonging to four orders were associated with 13 pest species in Casamance agro-ecological zone ( Table 2). Among these predators, species belonging to the Hemiptera were more abundant and their target pests were more diversified.

Parasitoids diversity
The host range of the parasitoids is determined to show the parasite complex associated with each pest.
A number of 14 parasitoid species were associated with a host range of 8 pest species in Casamance agro ecological zone (Table 3). Among these parasitoids, Hymenoptera is the most representative with 10 species found.

Natural enemies' diversity indices
Ecological indices are used to assess the diversity of natural enemies associated with pests in different localities (    (Table 4). The word "data" is plural, not singular.

Abundance of Natural Enemies of Pests
The abundance of natural enemies (predators and parasitoids) was compared between localities ( Table 5). The polyembryonic ovo-larval parasitoid, Copidosoma floridanum produces large numbers of individuals. Similarly, the larval parasitoid Euplectrus laphygmae is a gregarious ectoparasitoid that produces numerous individuals. The results show a significantly higher abundance of natural enemies in the localities of Ziguinchor and Bignona than in the locality of Oussouye (χ 2 = 384.218; df = 2; p < 0.0001) ( Table 5).

Determination of the Parasitism Rate
Natural pest control is determined by calculating the percentage of parasitism.
The parasitism rate of insect pests associated with crops is calculated according to the localities. The parasitism rate was calculated by dividing the number of parasitized larvae (determined by parasitoid emergence, excluding dead larvae without parasitoid emergence) by the number of larvae collected, expressed as a percentage. The percentage of regulation varies between 0 and 50% depending on the abundance of the pests and on the parasitoid species (Table 6).  Larvae = Number of collected larvae; P-Larvae = Number of parasitized larvae; % P = Parasitism rate. The parasitism rate was calculated by dividing the number of parasitized larvae (determined by parasitoid emergence, excluding dead larvae without parasitoid emergence) by the number of larvae collected, expressed as a percentage.

Discussion
The abundance of pests and the number of host plants found are more important in Ziguinchor than in Bignona and Oussouye. On the other hand, the number of pest species is lower in Oussouye followed by Ziguinchor and Oussouye.
The presence of host plants as food resources for these pests influences their abundance. The specific richness of host plants favours pest abundance. This result is confirmed by [12] who show that the species diversity of host plants influences pest abundance. In an agrosystem, the quality and quantity of available food resources favour the abundance of certain pest species. with alternative prey or hosts [14]. Nectar is a sweet resource that increases the longevity and oviposition period of a female parasitoid. The biodiversity of natural enemies is high in all three locations and is greatest in Ziguinchor. The presence of a high diversity of species shows an ecosystemic balance in the agroecosystems of Casamance. This balance is reflected in the high entomological diversity found. In fact, the agrosystems preserve the ecosystemic balance by maintaining the diversity of arthropods in the environment [15]. Among these arthropods, insects are important parts of the agrosystem alimentary chain [16] [17]. The abundance of natural enemies is greater in Ziguinchor. The percentage of regulation varies between 0 and 50% depending on the abundance of pests and the species of the parasitoid. This abundance can be explained by the crops grown. Indeed, Ziguinchor is the only locality where maize was found. This explains the unique occurrence of the maize pest Spodoptera frugiperda and its parasitoids Hexamermis sp., Chelonus sp., and Campoletis sp., which are the most abundant of those listed and only present in Ziguinchor. In addition, a gregarious parasitoid species Euplectrus laphygmae, and a polyembryonic species Copidosoma floridanum were found in Ziguinchor. This shows that the high abundance and diversity of natural enemies in Ziguinchor are due in part to the phenomenon of host fidelity and in part to the biology of the parasitoids. The phenomenon of host fidelity shows the influence of maize on natural enemies by the preferential choice of female parasitoids of the species Chelonus insularis and Campoletis sonorensis to prefer to stay and reproduce there [18].
This means that the presence of natural enemies depends partly on the crops grown. Indeed, crops are the first factor that alerts natural enemies through the volatile substances they secrete. When a plant is attacked by a pest, it releases volatile substances that attract the pest's natural enemies [19]. This result shows the existence of a tri-tropic interaction between plants, pests, and natural enemies. In an agroecosystem, the presence of a host plant favours the presence of the associated pest [12] [20] [21] and the presence of the pest favours natural enemies. Indeed, the host plant constitutes an indispensable food resource to maintain the pest in the environment. Similarly, pests are essential in a host-parasitoid relationship for the immature phase of the parasitoid, which is dependent on the host pest [22]. The Host plant is essential for the pests as the pests are indispensable for the natural enemies. According to the biology of the parasitoids found in Casamance, the abundance of natural enemies varies according to locality. The species Euplectrus laphygmae, found only in Ziguinchor and Oussouye, is a grega-  [23].
In addition, the parasitoid Copidosoma floridanum is one of the most extreme cases of polyembryony, producing up to 2.000 embryos from a single laid egg [24]. However, it was in Ziguinchor and Bignona that pest larvae parasitized by Copidosoma floridanum were more numerous than in Oussouye. This result explains the significantly higher abundance of natural enemies observed in Ziguinchor and Bignona compared to Oussouye. Predator Hemiptera and Parasitoid Hymenoptera have higher species richness. The presence of many species of predatory Hemiptera is explained by the availability of plant and animal food resources. Indeed, many Hemipteran predatory are zoo phytophagous. They are not only entomophagous [25] but also phytophagous [26]. The food resources of the predators including lepidopteran eggs and larvae, and plant species are very diversified and widely distributed in Casamance. This widens the range of food for these predators in the environment. Generally, predators are generalists as they feed on several insect pests. Their generalist function could partly explain their great success as a key biocontrol agent [27]. The presence of a very diverse flora in Casamance favours predatory Hemiptera. Parasitoid Hymenoptera is more specific in their relationship with their hosts than predators are with their prey. Indeed, parasitoids need a host to ensure their survival [22]. In parasitic Hymenoptera, the development of immature individuals depends at least once and necessarily on a host. The host constitutes a food resource and/or a protective shelter for immature individuals. Furthermore, Hymenoptera is known to be very successful parasitoids due to the presence of a piercing ovipositor [28].
In this work, a total of 25 species of natural enemies including 15 parasitoids and 10 predators contribute to the natural control of 13 pest species in the Casamance agroecological zone. Predatory Hemiptera and parasitoid Hymenoptera have higher species richness. Natural enemies are more abundant in Ziguinchor and Bignona than in Oussouye. The preservation of these natural enemies must be achieved through knowledge of their diversity and an understanding of trophic interactions with pests in order to develop biological control programs against crop pests and preserve the resilience of agro-ecosystems.