A survey of the insect pests and farmers’ practices in the cropping of yellow pepper Capsicum annuum Linnaeus in Enugu State of Eastern Nigeria

Yellow pepper (Capsicum annuum L.) is the second market gardening crop after tomato, and subsequently, a major source of income to farmers in Nigeria. Pests and diseases reduce yields and quality of marketable fruits. A study was conducted in Ibagwa-Agu, Lejja, Edem, Alor-Uno and EhaAlumona agro-based communities of Nsukka Local Government Area to assess the economic implications of insect infestation and control strategies on yellow pepper yield. Data on insect pests was collected using the modified Whittaker sampling techniques from July to September 2015, while farming practices and economic consequences of pest infestation were monitored using questionnaires in December 2015. A total of 2,279 insects comprising 10 pests and 2 predators were collected. Myzus persicae Sulzer (27.6% of total collections), Bemisia tabaci Genn. (21.1%), Aphis gossypii Glov. (14.1%) and Zonocerus variegatus Gestro(7.99%) were the four prominent insect pests, while Ladybird beetle larva of Harmoni axyridis (2.3%) and praying mantis Stagmonantis crolina (1.4) were the main predators encountered. Mean percentage of plants attacked and yield losses were significantly (P <0.05) lower in communities with a high percentage of farmers utilizing cultural control methods. A higher percentage of the farmers were females. Farmers in Edem, Eha-Alumona, Lejja, AlorUno and Ibagwa-Agu in Nsukka Local Government Area of Enugu State therefore experience enormous economic loss in yellow pepper cultivation from the infestation of insect pests. Communities with a high percentage of farmers practicing cultural control methods had fewer plants attacked, while the predators were also more abundant. Further research is needed to ascertain the efficacy of these cultural methods.


INTRODUCTION
Yellow pepper (Capsicum annuum L.) is a spicy fruit, consumed extensively at world level (Dias et al., 2013).It has both nutritive and medicinal values.Some health-related phytochemical compounds found in yellow peppers are important in preventing chronic diseases such as cancer, asthma, coughs, sore throats, toothache, diabetes and cardiovascular diseases (El-Ghoraba et al., 2013;Wahyuni et al., 2013).C. annuum also has antioxidant, anti-mutagenesis, hypocholesterolemic and immunosuppressive properties (El-Ghoraba et al., 2013), as well as inhibits bacterial growth and platelet agglomeration (Wahyuni et al., 2013).Consequently, yellow pepper is in high demand both by the general public and pharmaceutical companies (Nwankiti, 1981;Denton and Swarug, 2007).
In Nigeria, yellow pepper is the second market gardening crop after tomato (Assogba-Komlan et al., 2009), and it is a major income source for farmers.The Nsukka Area in Enugu State, eastern Nigeria, is especially important in the cultivation of yellow pepper as it has the environmental conditions suitable for its cultivation.Yellow pepper cultivation is the major and sometimes the only agricultural activity of rural women in the State.Yellow pepper production in Nigeria has been facing many biotic and environmental constraints.Prominent among such constrains are pests and diseases which reduce yields and quality of marketable fruits (Echezona and Nganwuchu, 2006) In the tropics, particularly in Nigeria, some insect pests are directly associated with yellow pepper damage and yield losses, while others are important as vectors of diseases (Khan et al., 2009;Segnou et al., 2013;Zhani et al., 2013).
Information on the insect pests and farmers' practices in the cultivation of yellow pepper in Nsukka area is lacking.
This survey was conducted in some major yellow pepper producing communities in Nsukka Area to assess the status of yellow pepper production with a view to address production problems related to insect pests.The survey had the objective of (i) identifying through questionnaire, technologies which influence insect spread and damage and (ii) identifying through field sampling major yellow pepper insect pests and their spread.

Study area
The Nsukka Local Government Area (6°5ꞌ 24ꞌꞌ N and 7°23ꞌ45ꞌꞌE) is located in the northern part of Enugu State in south-eastern Nigeria.The study was conducted between June and July, and December (2015) in five agro-based communities: Ibagwa-Agu, Lejja, Edem, Alor-Uno, and Eha-Amluona, chosen based on the following criteria: (i) relative importance of the yellow pepper crops in the communities, and (ii) its level of production.The average annual temperature falls between 27 and 28°C and average annual rainfall is about 1600 mm.The natural vegetation of the area is a derived savannah type and the trees found are usually drought resistant (Ugwu, 1964).Inhabitants in the Nsukka area have agriculture as their main source of income, being yellow pepper the main crop with economic importance.

Ethical consideration
Consent was obtained from the University of Nigeria ethical committee.The respondents were acquainted with the purpose of the study and assurances of confidentiality and anonymity were given to them.

Insect collection: Whittaker sampling protocol
Twenty (20) yellow pepper farms were chosen each from the five agro-based communities, making a total of 100 farms, using systematic random selection.A total of 310 m 2 per farm were sampled using the modified Whittaker sampling protocol (Whittaker, 1972).Whittaker plots (20x50 m) were centrally outlined with wooden pegs, threaded with rope, at each farm.Nested in each plot were ten 0.5x2 m subplots systematically spaced along the inside border, two 2x5 m subplots in alternate corners, and a 5x20 m subplot in the center of the plot.Fifty plants were sampled randomly from the mapped out area in each of the sampled farmlands, 30, 10 and 10 from the 5x20, two of the 2x5 m and ten 0.5x2 m subplots respectively.Handpicking and insect sweep nets were used to collect the insects.Collection was biweekly and at the morning and evening hours when the insects were less active.
Observations were made on leaves, stems and fruits for insects and insect damage.Percentages of plants damaged by insects per farm were calculated.Insects' samples were identified in the field and the laboratory with a hand lens and a microscope, using picture vouchers and specimens in the museum in the Department of Zoology and Environmental Biology, University of Nigeria, Nsukka.Insects with mean percentage abundance of above 6% were regarded as prominent.

Knowledge/attitude of farmers and socio-economic impacts of insect pests of C. annuum: Descriptive survey method
The study population consisted of the twenty farmers whose farms were sampled for insect pests and an additional twenty randomly selected, in each community, making it a total of 200 respondents.The farmers' knowledge on insect pests of yellow pepper, yield losses from the insects and farming practices used to control them, were investigated using descriptive survey method, involving interview questions administered as semi-structured questionnaire.The interview questions were coined from 4 research questions: 1.Is yellow fever cultivation the major source of income amongst the farmers?; 2. What is the level of knowledge of the farmers of insect pests of pepper?; 3. What are the economic impacts of insect pests on Capsicum annuum on farmers in Ibagwa-Agu, Lejja, Edem, Alor-Uno and Eha-Alumona agro based communities of Nsukka Local Government Area? ; 4. What are the insect pest control methods practiced in Ibagwa-Agu, Lejja, Edem, Alor-Uno and Eha-Alumona agro based communities of Nsukka Local Government Area?
Author(s) agree that this article remain permanently open access under the terms of the Creative Commons Attribution License 4.0 International License  26-30, 31-35, 36-40, 41-45, 46-50, 51-60 and <60 years.Metrics assessed through questionnaires are expressed in percentages.The questionnaires were administered in December, 2015 after the major harvesting periods.Yield reduction of above 25% was regarded as high, while cultivation period of above 5 years was regarded as long duration.

RESULTS
In all the communities where the survey was conducted, females than males were involved in the production of yellow pepper as follows,55:45; 65:35; 765:36; 70:30 and 75%:25% for Edem, Lejja, Eha-Alumonah and Ibagwa Agu, respectively) (Table 1).Females between the age range 31-50 years were most involved in yellow pepper cultivation than other ranges (Table 1).Yellow pepper cultivation was the major source of income for all the farmers interviewed (100%).Manual farming was the most common and major method of farming (100%).The farmers had cultivated yellow pepper for periods ranging from 6 to 30 years (data not presented).
Income generated annually ranged between N100,000 and 900,000, with 41% of the women earning between 800.000-900,000, while 20% of the men were found in this income range (data not presented).
In all locations, all the farmers experienced yield loses due to insect infestation (100%).80%farmers in Ibagwa-Agu experienced about 26 to 50% yield reduction, while 20% experienced 51-75% yield reduction.Most farmers in Alor-Uno (91.9%) also experienced 26 to 50% farm yield reduction, while 8.1% experienced 51-75% yield reduction.Those 100% farmers in Eha-Alumonah experienced lower yield reduction (about 1 to 25%) farm yield reduction.Most farmers in Lejja, 44, 50 and 5.6% experienced between 1 to 25%, 26 to 50% and 51 to 75% farm yield reduction respectively.Those in Edem  experienced 1 to 25%, 26 to 50% and 51 to 75% yield reduction in the proportions of 43, 43.29 and 13.8% respectively (Figure 1).No farmer experienced farm yield reduction between 76 to 100%.There was a significant different in the level of farm yield reduction experienced during the time of infestation (P < 0.05) in Lejja, Eha-Alumonah and Alor Uno.No significant different existed between the level of farm yield reduction in Edem (P > 0.05).Chemical control strategies were used extensively by the farmers and more by the male farmers than the female farmers (88.8:81.8; 100:73; 100:42.31; 100:79.29;100:86.6%for male and female in Edem, Lejja, Eha-Alumonah, Alor -Uno and Ibagwa Agu respectively).The farmers used both organic based insecticide(applying palm head husk ashes to the stem and leaves of the plant and application of aqueous extract of leaves and roots of Azadiracta indica which were majorly their traditional control strategies) and inorganic based insecticides(spraying a combination of detergent and kerosene mixed with water, DDT, Cypermethin etc).A higher number of female farmers used the organic insecticide (68.18:0; 30.77:0; 30.77:28.57;22.14:0 and 66.67:0% for female and male in Edem, Lejja, Eha-Alumonah, Alor-Uno and Ibagwa Agu respectively).The cultural control strategies were also practiced more by the females than the males (18.18:11.11;15.39:0; 57.69:0; 13.57:0 and 13.33:0 for female and male in Edem, Lejja, Eha-Alumona, Alor Uno and Ibagwa Agu respectively.some traditional cultural methods most utilized were Early harvesting of crops where peppers were harvested while they were still green to minimize the effects of rot and fruit cracking, manuring using goats and cow dung, farm sanitation and crop rotation (Table 5).
In the locations, more farmers (71.16-93%) significantly (P < 0.05) used chemical treatments, while only 6.66-28.84%applied cultural methods.Chemical control methods were most utilized in Alor Uno, followed by Ibagwa Agu, and Lejja, while cultural control was most utilized in Eha-Alumona, followed by Edem, and Lejja.
More plants were significantly (P < 0.05) attacked in communities with a high chemical control (CH) and low cultural control methods (CC).Thus the highest number of plants attacked (48%) by insects was encountered in Ibagwa Agu, followed by Alor Uno (41%), Edem (32%), Lejja (29%) and Eha-Alumona (27%) with CH to CC ratio of 93:6.66;98:6.78;85.3:14.7;89:15.37 and 71.16:28.84%.The number of pests was higher in communities with high CH and low CC.In communities with high number of predators, lower number of insect pests was encountered, while communities with lower number of predators, higher number of pests was collected (Table 6).

DISCUSSION
The survey of farmers' practices in the cropping of yellow pepper revealed that yellow pepper cultivation was the main source of income of the farmers.Indeed in Nigeria, yellow pepper is the second market gardening crop after tomato (Madu et al., 2005;Assogba-Komlan et al., 2009).In this study, income generated from yellow pepper cultivation was N100,000 to 900.000 annually.The cash potentials from this study, combined with previous studies indicating that it is easy to grow, harvest and process, make yellow pepper suitable for use in poverty reduction (Dagnoko et al., 2013).In all the communities sampled a higher percentage of the farmers were females, making women a crucial resource in agriculture and rural economy (FAO, 2011).
The insect pests of yellow pepper probe from Enugu State yielded a greater number of Hemiptera collections than the other orders of insects.Four species belonging to the order Hemiptera were found viz; M. persicae, A. gossypi, B. tabaci and H. schoutedeni, while two were Coleopterans (N.sjostdi and E. albovittata), one species for Orthoptera and Diptera each (Z.variegatus and Zonosemata spp.respectively).One Lepidoptera, B. betularia and Thysanoptera, S. dorsalis were collected.Praying mantis and Ladybird beetle H. axyridis were the only predators collected.Insect pests have been reported as the main biotic constraints of yellow pepper cultivation (Ingerson-Mahar et al., 2015;Seal and Martin, 2016).Of the 10 insect pests identified, four: M. persicae, B.tabaci, A. gossypii, and Z. variegatus were the prevalent and therefore the major pests of yellow pepper in Nsukka agro-based communities sampled, while H. schoutedeni, N. sjostedi, S. dorsalis, E. albovittata, B. betularia and Zonosemata spp were minor pests.This is at variance with an earlier report where H. schoutedeni and N. sjostedi were the prevalent insest pests of pepper, while Z. variegatus was a minor pest (Echezona and Nganwuchu, 2006).
M. persicae which was observed attacking roots, in earlier studies, has been reported as being ubiquitous and attacking nearly130 plant families including pepper (Uzo and Williams, 1989;Helmet, 2013).It causes decreased growth, shriveling of the leaves and the death of various tissues, in addition to transmitting leaf coil and growth distortion denoviruses (Van Munster et al., 2013), while white flies B. tabaci, observed attacking leaves and  flowers in this study, have also been reported as vectors of viruses, all of which have led to loss in plant yield (Ingerson-Mahar et al., 2015).B. tabaci (silver leaf white fly) is one of the most destructive pests of mainly vegetables and ornamental crop world-wide and has vast host range, polyvoltinism, and short generation time, ability to transmit important plant viruses have contributed to its enormous damage potential (Shadmany et al., 2013).
In addition, B. tabaci, is a cryptic species complex with at least 32 biotypes based on the 3.5% divergent limit of the partial mitochondrial cytochrome oxiase subunit 1 (mt CO1) sequence (Dinsdale, 2010;Chowa-Reddy et al., 2012).Among all biotypes, B and Q are the most invasive and the huge losses caused by this pest are almost always associated with these biotypes (Chowa-Reddy et al., 2012).In many cases upon introduction into a region, they establish and partially or completely displace indigenous biotypes (Rao et al., 2011).Both invasive biotypes have already invaded and continue to invade many other countries around the world.Timely identification of the biotypes in Nsukka area can help prevent or reduce huge economic loses.Further studies are recommended to ascertain the biotype(s) in Enugu State and if it is the invasive Q type, quarantine measures can be used to hinder or delay its further spread into other States in Nigeria.
A. gossypii which was found on the shoot of the yellow pepper plants has been earlier reported as a major pest of many crops including pepper and transmits over 50 plant viruses (Blackman and Eastop, 2006).
Z. variegatus was collected from the shoot of the pepper plants in this study and previous studies report Z. variegatus as an important polyphagous pest of vegetable and food crops in West and central Africa and in Nigeria, yield loses have been recorded for various crops, including pepper and outside physical damage to leaves and shoots, it also transmits viruses and bacteria (Modder, 1986).
Helopeltis schoutedenti, E. albovittata, S. dorsalis, N. sjostedti collected from shoots (first three pests) and leaf (last pest)have been reported to feed on shoots, branches or whole plants and are known to cause crop failure all over the world, larvae of B. betularia and Zonosemata spp found in pepper fruits in this study, breed in pepper fruits causing enormous fruit lose (Helmet, 2013).
M. persicae and B. tabaci were more abundant in Ibagwa Agu and Akor Uno than any of the other three sampled communities and may account for the higher number of plants attacked and subsequent loss in yield in this sturdy.In Ibagwa Agu, all the farmers suffered from very high yield loss, 80 and 20% suffered from 26-50% and 51-75% respectively, while in Alor Uno, crop yield loss was also high, 91.9% and 8.1%.Yeild loses were lower in Edem, Lejja and lowest in Eha-Alumona, and this correlated with the lower percentage of plants attacked.Lower numbers of the major pests may also have accounted for this reduction in yield lose.This explanation may be plausible for Edem and Lejja, but not for Eha-Alumonah.In Eha-Alumonah, higher numbers of the major insect pest were encountered than Edem and Lejja, but fewer plants and yield loses were recorded in Eha-Alumonah than Lejja and Edem.This may be as a result of the presence of a higher number of the predatory insects in Eha-Alumonah, H. axyrids (28.3%) and Stagmonantis carolina (29.0%), when compared to the lower numbers in Edem (18.9:22.6% and 18.9:22.6%for H. axyrids and S carolina for Edem and Lejja respectively).Furthermore, the two communities (Edem and Lejja) with the highest number of plants attacked had the lowest number of predators (Table 3).Communities with high number of predators had low number of the insect pets.The predators may have eaten some of the insect pests reducing their numbers.Praying mantis have been reported in previous studies as large insects that feed on beetles, grasshoppers, wasps, bees, and any insect they can catch Bodson (2014), while H. axyridis preys on aphids and scale insects (Emden, 2011).Chemical and cultural practices were the major control methods utilized by farmers in these communities in this study.The survey also showed that most of the farmers use insecticides to mitigate pests.Chemical insecticides therefore, seems to be the popular pest control method among famers.In assessing the pest management techniques among farmers in Cameroon, West Africa, 92% of the farmers used synthetic pesticides (Abang et al., 2014).
The chemicals utilized for chemical control included organic and inorganic based chemicals.The inorganic based chemicals were DDT, Cypermethrin, detergent and kerosene solution, etc., while the inorganic based chemicals control strategies which were mostly their traditional control methods were Elaise guinensis husk ashes sprinkled on the stem and leaves of the plant, aqueous extracts of leaves and seeds of neem sprayed on the plants.Some of these strategies are already being utilized such as soap solution which was reported to be effectively used in the control of A. gossypii (Blackman and Eastop, 2006).The use of wood ashes sprinkled around yellow pepper plants and other vegetables kept away caterpillars and was reportedly used to control insectsin ealier studies (Golob and Webley, 1980).The water extracts of the seeds and the leaves of neem tree were also previously reported by Suhmutter et al. (1984).In addition, in all the localities sampled, more farmers utilized inorganic based insecticides than organic.This study also revealed that communities with high percentage of farmers utilizing chemical control, experienced higher insect pest attack on plants and higher yield loss, and lower numbers of predatory insects.The insects may have become resistant to the insecticides as reported for B. tabaci which has developed resistance against almost all groups of insecticides (Rao et al., 2011).Synthetic chemical insecticides have also been reported as affecting nontarget organisms.In this study, non-target organisms such as the predators may have been killed by the insecticide, reducing their numbers and off course the number of insect pests eaten.Furthermore, exposure to pesticides is one of the most important occupational risks among farmers in developing countries (Wesseling et al., 2001;Konradsen et al., 2003).Hepatic dysfunctions (El-Demerdash et al., 2001), nephrotoxic effects such as cholinesterase inhibitor poisoning have been reported (Zahm and Blair, 1992).Cancer and even death are more frequent among farmers than the general population (Gertrudis et al., 2001;Mansour, 2004).Furthermore, cytogenetic studies showed an increase in DNA damage and higher chromosomal aberrations (CAs) in exposed farmers compared to the control subjects (Naravaneni, 2007.These adverse effects from synthetic chemical insecticides mandates farmers to explore other ecofriendly, safe and efficacious insect pest control strategies such as organic based traditional chemical control methods and cultural methods.Further studies are necessary to determine the efficaciousness of the traditional organic base chemical control strategies. A diverse number of cultural methods were used by some of the farmers in this study to control pests, these were early harvesting of crops, (a traditional method of pest control where crops were harvested while they were still green to minimize the effects of rot and fruit cracking).This method also prevented damage by fruit worms which attack pepper fruits when they begin to ripen.In the study also, some farmers claimed that chicken droppings, goat and cow dung have proved useful in plant protection, when sprayed on all green plants of vegetable and fruits.Earlier studies revealed that while the use of animal excrement may increase soil nutrient, and subsequently, increase plant growth, increased rates of poultry droppings, increased aphids (except B. tabaci), mired and grasshopper infestations as well as incidences and severities of pepper venial mottle virus (PVMV) symptoms, compared to where no manure was applied; but not (Echezona and Nganwuchu, 2006).Chicken droppings may have selective effects on the insect pests.In this study, the lowest percentage reduction in yield was from the community utilizing the highest percentage of cultural control (Eha Alumnoah).Further studies are needed to ascertain the efficacy of these control measures, indicating the pests that can be effectively controlled by the measure as was indicated for chicken droppings.And also the effects of the cultural control methods on non-target insects especially the predators.
The survey also showed some perceptional gender differences in the derived savannah zone of Eastern Nigeria.Males perceived the pest incidence with an equal importance, while females recognized Z. variegatus as one of the major pests.Males used vague attributes like harmful or harmless, while females were more specific e.g gave vivid description of Z. variegatus biting off the shoot of the young transplanted pepper plants.A higher percentage of the females used the cultural control methods more than the males such as sprinkling of ash on shoots and leaves, spraying with goats and cow dung, early harvesting, farm sanitation and crop rotation, while the males used chemical insecticides to control the insect pests more frequently.This choice of cultural control amongst the females was not in recognition of the reduced impact on non-target organism, or its sustainable and environment safety measures, but because it was cheap and also easier to use.The females who could afford chemical insecticides used them.A higher number of females than males also observed that yellow pepper farms close to herbaceous fallows were attacked by greater number of Z. variegatus than those far away from them and close to the forests.Herbaceous fallows provide favorable breeding sites for Z. variegatus (Modder, 1986).This observation made the fallow cultural farming system unpopular among farmers, while crop rotation was encouraged.Crop rotation is the practice of growing a series of dissimilar or different types of crops in the same area in sequential seasons.Among other advantages, it mitigates the build -up of pathogens and pests that often occur when one species is continuously cropped (Francis, 2003).This is especially important as the study revealed that yellow pepper was not intercropped with other crops, therefore monoculture was the major practice among the farmers and pests population and pathogens are commonly built up in mono culture unlike in polyculture (Francis, 2003).Crop rotation is one component of polyculture and should be encouraged amongst the farmers.

Conclusion
It is evident from the investigations, that the farmers in Edem, Eha-Alumona, Lejja, Alor-Uno and Ibagwa-Agu in Nsukka Local Government of Enugu State experience enormous economic loss in yellow pepper cultivation from the infestation of insect pests.Most of them use chemical methods to mitigate insect pests, while only a few, which were mostly females utilize cultural methods.Some of the communities with a high percentage of farmers practicing cultural control methods had fewer pest and plants attacked, while the predators' numbers were also higher than communities with fewer farmers utilizing cultural control methods.Further research is needed to ascertain the efficacy of the cultural methods.Given the wide array of human health effects from pesticide exposure, cultural control measures should be encouraged, especially crop rotation to avoid a build-up of pests and pathogens.

Figure 1 .
Figure 1.Farmers' perception of percentage reduction in yield from insect infestation in 2015 from the previous year (2014).

Table 1 .
No of farmers' using yellow pepper cultivating as their major source of income in the agro-based communities.

Table 2 .
Insect pests and predators collected from yellow pepper plants in the sampled agro-based communities.

Table 3 .
Insect pests and number collected from C. annuum(Yellow pepper) from the agro-based communities.

Table 4 .
Level of knowledge of the farmers on insect pests of yellow pepper in the agro-based communities

Table 6 .
Effects of control methods on the numbers of predatory insects, predominant insect pests and plants attacked in the agro-based communities.
*Field observations.CH = Chemical Control method; CC= Cultural Control method; NC = No Control.