Citrus Insect Interactions: Implications for Pest Management

Journal of Agriculture and Ecology Research International 8(3): 1-10, 2016; Article no.JAERI.25842 ISSN: 2394-1073

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Owusu Fordjour Aidoo 1*, Clement Akotsen-Mensah 1,2 , Rosina Kyerematen 1,3 and Kwame Afreh-Nuamah 1,2

1African Regional Postgraduate Programme in Insect Science, University of Ghana, Accra, Ghana. 2Forest and Horticultural Crops Research Centre, School of Agriculture, College of Basic and Applied Sciences, University of Ghana, Ghana. 3Department of Animal Biology and Conservation Science, University of Ghana, Ghana.

Authors’ contributions

This work was carried out in collaboration between all authors. All authors read and approved the final manuscript.

Article Information

DOI: 10.9734/JAERI/2016/25842 Editor(s): (1) Abdel-Tawab H. Mossa, Environmental Toxicology Research Unit (ETRU), Pesticide Chemistry Department, National Research Centre, Egypt. Reviewers: (1) Shravan M. Haldhar, ICAR-Central Institute for Arid Horticulture, Bikaner, India. (2) Ilias Faiza, Center university of Belhadj Bouchaib, Ain Temouchent, Algeria. (3) Peng He, Guizhou University, China. Complete Peer review History: http://sciencedomain.org/review-history/15003

Received 22 nd March 2016 Accepted 4th June 2016 Original Research Article th Published 13 June 2016

ABSTRACT

We observed that insect interactions lead to damaged fruits, leaves, stems, and exposed fruits and tree trunks to pathogenic infection, however, some citrus trees were protected by these interactions. Our study shows that Oecophylla longinoda and Crematogaster spp. protect citrus aphids and citrus scale insects from their natural enemies leading to their outbreak and further damage to the citrus plant. Citrus trees with more Oecophylla and Crematogaster had fewer pests such as fruit flies, termites and the variegated grasshopper, Zonocerus variegatus . Our study shows that “chain” formation by weaver ants, Oecophylla enables them to reach the same colony in different citrus trees. We identified wild passion plant, Passiflora sp. as an alternate host for Leptoglossus spp. We recommend Oecophylla and Crematogaster as biological control agents against fruit flies, termites and the variegated grasshopper; however, they could lead to an outbreak of citrus aphids and citrus scale insects. Phasmomyrmex aberrans is antagonistic to

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*Corresponding author: E-mail: [email protected];

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Oecophylla and so in an attempt to utilize Oecophylla as a biological control agent, we recommed that care must be taken to ensure that they do not come together. As biological control agents in orchards that do not have closed canopies, we recommend that sticks or ropes be connected to adjacent trees to facilitate movement of the ants to enhance their dispersal in orchards . Care must be taken to clear all Passiflora sp. from citrus orchards.

Keywords: Insect predation; Oecophylla; in; fruit flies; insect damage.

1. INTRODUCTION constraints, the most important are insect pests because, if not controlled, insect pests can Citrus belongs to the family Rutaceae and is an completely devastate crops through transmission evergreen, aromatic, broad-leaved tree which of virulent disease pathogens and direct feeding produces fruits of different sizes and forms. It is a on the marketable fruits. major fruit crop grown worldwide, widely distributed and performs well in a wide range of The objective of the study was to identify insect soils, however, it does not tolerate waterlogged pests of citrus, damage caused by these pests, soils and grows well in freely draining, acid to and their interactions with other species based neutral soils with pH ranging from 5-8. It is mainly on field observations to help provide cultivated in parts of tropical and sub-tropical economically sound integrated pest management regions of the world. In Ghana, citrus has been option for citrus in Ghana. cultivated since 1913 [1] in areas which experience bimodal rainfall patterns but below 2. MATERIALS AND METHODS the production potentialities of the country [2]. The origin of citrus is not known [3]; however, its 2.1 Study Area history reveals that it must have originated from South-eastern Asia, Southern China and possibly Our study was carried out for a period of seven North-eastern India [4]. months from September 2013 to March 2014 in A wide variety of insects are associated with citrus orchards (monoculture) in the semi- citrus trees with each having its preferred feeding deciduous rainforest and coastal savannah parts like fruits, stems, branches, leaves and agroecological zones of Ghana. In both orchards, flowers. Some insects in the citrus plantation are weed management was by the use of machetes, pests and cause damage to the citrus fruits. For both farms were wholly organic and the citrus instance, Bactrocera spp. and Ceratitis spp. variety was Late Valencia. In the semi-deciduous (both fruit flies) puncture the fruits and lay their rainforest zone, the research was carried out in eggs into them; hence, inducing false ripening the citrus plantation (CI. 25) of the Forest and and subsequently fruit drop [5]. Insects which are Horticultural Crops Research Centre not pests are also present and serve as a source (FOHCREC) at Okumaning, Kade in the of food for the beneficial insects and some also Kwaebibirem District of the Eastern Region of contribute to the recycling of waste into nutrients Ghana. This area experiences an annual bimodal for the citrus trees. After citrus establishment, rainfall pattern ranging between 1200-1300 mm, arthropod species colonize and over time temperature range of 25-38°C [7]. The ꞌ progressively increase in diversity and coordinates of the site are N 06°09.473 , W 000 ꞌ abundance. 54.550 and E: 552’. The orchard was established 20 years ago with a triangular The productivity and sustainability of the citrus planting distance of 6 m x 6 m. The vegetation in industry in Ghana has been characterized by a the study site mainly consisted of Panicum number of production constraints including the maximum and Pueraria phaseoloides . In the high cost of inputs such as fertilizer, harvesting coastal savannah zone, the research was carried machinery and processing, pesticides, out in a farmer’s plot at Asuansi Agriculture marketing, diseases and pests to mention a few. Research Station in the Abura/Aseibu/ Besides, pests, diseases, poor marketing of Kwamankesse District of the Central Region of citrus fruits, lack of certified rootstock, lack of Ghana. The area experiences a mean annual proper extension delivery, complexities of land rainfall of 980 mm and the rainfall pattern follows tenure system, lack of irrigation facilities and the bimodal distribution. Mean monthly post-harvest losses are observed to be major temperature is about 26.90°C [6] and the constraints [6]. Among these production coordinates of the study site are N 05° 18.654 ꞌ,

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W 001° 15.667 ꞌ and E: 363 ft. The citrus orchard as biological control agents Phasmomyrmyx was established 15 years ago with a triangular should be eliminated to avoid competition for planting distance of 7 m x 7 m. The predominant resources. Insects drive away less dominant vegetation of the study site mainly consisted of species when they are together and this occurs Chromolaena odorata and Panicum maximum . either between insects of the same species belonging to different colonies or insects 2.2 Data Collection belonging to different species. For instance, in two cases, fruit flies (Ceratitis ditissima and Visual observations of insect interactions were Bactrocera invadens ) that were observed on the recorded in two different citrus orchards. Citrus same tree as O. longinoda were attacked and leaves, flowers, trunk, fruits and the vegetation in driven away whenever they attempted to get the understory were observed for the following close to the fruit flies (Fig. 2a, b). The association parameters; predation, antagonism, foraging and between Macrotermes spp., O. longinoda and feeding, nest distribution, co-existence, the spiders was antagonistic; however, they were mating of insects and insect interaction with able to occupy the same habitat as long as they spiders and mites. The observations were made exploited different resources. In one observation, in the morning, afternoon and evening periods. the spider protected itself by hiding in its web Insects were collected using forceps and aerial blending into the bark of the host tree making it net, stored in 70% ethanol, sorted and identified difficult to be detected by the O. longinoda and to the lowest taxonomic rank possible. A digital Macrotermes spp., Macrotermes spp. on the camera was used to take photographs of the other hand hid in their runways or tunnels on the insects. citrus tree and O. longinoda were observed moving up and down patrolling the citrus tree 2.3 Insects Identification (Fig. 3). Citrus trees with more of either Crematogaster spp. or O. longinoda had fewer or no citrus pests such as Leptoglossus spp., Insects were identified with reference to Ceratitis ditssima, Bactrocera invadens and collection in the museum of the Department of Dacus spp. hence little or no damage by these Animal Biology and Conservation Science pests to citrus. Citrus trees with more of either (DBCS), University of Ghana, Legon as well as O. longinoda or Crematogaster spp. had no with reference to [8-13] and Aidoo et al. [14]. Dr. praying mantids ( Mantids religiosa and Maxwell K. Billah of DABCS helped in the Sphodromantis spp.) indicating possible identification of the fruit flies. The voucher antagonism between natural enemies which specimens were deposited at the African could be affecting the predatory behaviour of Regional Postgraduate Programme in Insect praying mantids in the orchards. This confirms Science (ARPPIS), West African Sub-Regional earlier findings by [15] who made an observation Centre, University of Ghana, Legon. on antagonistic behaviour between insects

3. RESULTS AND DISCUSSION associated with oil palm plantations in Ghana. Table 1 shows some insects observed showing On five separate occasions, we observed that antagonistic behaviour during the study period. insects of different species as well as insects of the same species but belonging to different 3.1 Co-existence of Insect Species colonies competed for resources such as food and habitat leading to fighting with eminent death In several cases, many insects belonging to or elimination of the less dominant species. For different species were observed occupying the example, Phasmomyrmex aberrans from one same habitat without being antagonistic towards citrus tree were observed attacking Oecophylla each other. For example, Crematogaster spp. longinoda from a different citrus tree (Fig. 1). and citrus aphids ( Toxoptera aurantii and These attacks went on for more than three hours Toxoptera citricidus ), O. longinoda and citrus before all the O. longinoda were totally removed aphids, and O. longinoda and citrus scale insects from the tree. A lot of deaths were observed, (Lepidosaphes beckii ) (Fig. 4) were observed however, O. longinoda recorded the higher together without attacking each other . mortalities compared to P. aberrans in a ratio of O. longinoda and Crematogaster spp. are 1:10. This shows that O. longinoda and predators of natural enemies of citrus aphids and P. aberrans are antagonistic torwards each other citrus scale insects were found tending citrus and in a situation where Oecophylla which are aphids and scale insects, thereby, protecting natural enemies of pests of citrus are to be used them from their natural enemies leading to more

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damage caused by aphids and scale insects to temperature. The observations were made in the the citrus trees.Citrus trees with O. longinoda vegetation of the understory of the citrus trees, and Crematogaster spp. which had more citrus however, a few insects were observed mating in scale insect and aphid infestation. This the canopy of the citrus trees. Z. variegatus was observation is consistent with earlier findings that found mating on each field visit during the seven- mutualism mostly exists between ants and month study period. Two main mating positions honeydew producing insect pests such as aphids were observed in the field. Among the and scale insects and such mutualism leads to Hymenoptera and Coleoptera, male insects were increasing abundance, damage and deterring of found mounting the female from behind (Fig. 5a). predation by their natural enemies Hill et al. [16]. The males and females of robber flies, butterflies Zonocerus variegatus , Leptoglossus spp. and and moths were observed mating head to the fruit flies were observed together on the same abdomen. Mating positions were dependent on citrus tree not fighting each other. Z. variegatus the species involved while the duration of mating are defoliators and feed on citrus leaves, varied depending on the disturbance around the Leptoglossus spp. puncture and feed on unripe vicinity they were mating in. On three separate citrus fruits whilst fruit flies puncture and lay their occasions, Sagra femorata was observed mating eggs in unripe citrus fruit leading to false ripening for more than 40 minutes whereas Lycus and subsequent fruit drop. The co-existence of trebeatus was observed mating for more than 30 these pests observed on a single citrus tree minutes (Fig. 5b, c, d). resulted in both loss of more leaves and damaged fruits. These findings were consistent Table 2. Co-existence of insect species with Afreh-Nuamah [5], that earlier reported Z. variegatus , Leptoglossus spp. and fruit flies as Species A Species B the major pests of citrus in Ghana. Some insects Oecophylla = Tetramorium spp. observed co-existing without fighting are shown longinoda in Table 2. Leptoglossus spp. = Toxoptera aurantii, Toxoptera citricidus, Table 1. Antagonism of insect species Aphis gossypii Zonocerus = Leptoglossus Species A Species B Ceratitis spp. = Toxoptera aurantii, Oecophylla longinoda ≠ Crematogaster Toxoptera citricidus, spp. Aphis gossypii Oecophylla longinoda ≠ Zonocerus Zonocerus = Bactrocera invadens, variegatus varigatus Dacus sp. and Crematogaster spp. ≠ Zonocerus Ceratitis ditissima. variegatus Lepidoptera (Caterpillar) ≠ Oecophylla 3.3 Feeding and Its Effect on Citrus longinoda Leptoglossus spp. ≠ Oecophylla Both the nymph (Fig. 6a) and adult (Fig. 6b) of longinoda Z. variegatus were observed on several Coccinelids ≠ Oecophylla occasions feeding on both fresh and old leaves longinoda of citrus, although, they preferred the younger, Camponotus spp. ≠ Coccinellids softer leaves. Several leaves were fed on and Oecophylla longinoda ≠ Mantis religiosa defoliated by these grasshoppers, thereby, Crematogaster spp. ≠ Leptoglossus reducing the surface area exposed for spp. photosynthetic activity, however, the damage did Crematogaster spp. ≠ Coccinellids not affect the yield of the citrus when compared to those without grasshoppers as there were still 3.2 Mating and Mating Behavior a lot of ripe fruits on the trees the grasshoppers fed on. The larvae of the citrus leaf miner, Most of the insects were observed mating in the Phyllocnistis citrella were observed feeding on morning and evening hours when temperatures citrus leaves creating “serpentine mines” on both and humidity were low and high, respectively. the upper and the lower surfaces of the leaves This could most probably be due to unfavourably (Fig. 7). Many of these larvae were observed in hot weather conditions during the afternoon the rainy season during the flush periods of the periods. This confirms an earlier report by Fazal citrus. Some ants such as Camponotus spp., et al. [17] that the rate of reproduction and Crematogaster spp., Tetramorium spp., and development of species is regulated by O. longinoda were also observed feeding on

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unopened flower buds until the buds decayed. stretch their heads to be able to reach them and This led to the abortion of the flower buds prior to complete the chain. Materials such as food and fruit formation (8a, b, c, d). The ants are mostly a larvae are then carried by workers of one tree nuisance to farmers during weeding and and moved on the chain to the other tree harvesting of citrus fruits. The findings, however, enabling the ants to move from one tree to agrees with [18] who reported that insects’ another. The only hindrance faced by the ants feeding causes damage to flowers, and flower was the wind which would sometimes blow some buds and reduces bud production and bud burst. of the ants forming the chain away thus Lepidopteran larvae (Fig. 9) were also observed disconnecting the chain (Fig. 15). feeding on citrus leaves until the whole leaf was completely defoliated. The larvae moved from 3.5 Insect Predation leaf to leaf and continued to feed till feeding was disrupted by disturbance around it. Fruit flies Insects were observed on twelve separate were observed on three separate occasions occasions preying on various life stages of other feeding on citrus fruits. Female fruit flies, different insect species and associated Ceratitis detissima puncture citrus fruits with its arthropods. For example, two different species of ovipositor and deposit their eggs into it leading to Asilidae (Robber flies) were found preying on premature ripening and subsequent fruit drop some Dipterans (Fig. 16a), Hymenopterans (Fig. 10). A grub of a beetle was observed (Fig. 16b) and spiders (Fig. 16c). O. longinoda feeding on a citrus tree resulting in the death of was observed preying on millipedes (Fig. 17a), the affected part (Fig. 11a, b). Macrotermes spp. beetles (Fig. 17b) and spiders (Fig. 17c) in the were observed on two different occasions orchard. In one case, O. longinoda were feeding on the branch of a citrus tree, ultimately observed transporting Macrotermes spp. leading to the death of the affected part (Fig. 17d) and Camponotus spp. (Fig. 17e) to (Fig. 12a, b). The termites also made tunnels in their nests. It became obvious that O. longinoda the trunk which led to secondary infection by the was a common predator of many insects and pathogens Lasiodiplodia natalensis or other arthropods as earlier reported by Van Mele Phytopthera spp. (Fig. 13). Some of the trees [19] and Ativor et al. [20]. O. longinoda attack were observed to have died due to the feeding of prey either individually or as a group. After the the termites and the subsequent onset of immobilization of their prey, other members of gummosis. Drosophila was also observed the colony join in an attempt to transport the prey feeding on rotten citrus fruits (Fig. 14). to the nest (Fig. 17f). O. longinoda was observed attacking Lepidopteran larvae; O. longinoda 3.4 Foraging of Insect Species workers surrounded and bit it and grasped its extremities, and at the same time began pulling O. longinoda and Crematogaster spp. were it. It was immobilized through prolonged observed on two occasions foraging both in the stretching and this rendered the caterpillar canopy and the understory of the citrus trees. It immobile. In the first instance, more O. longinoda was observed that rainfall affected the foraging workers were recruited due to the bigger size behaviour of most insects in the orchards by and aggressiveness of the prey. On the second delaying their activities particularly those of observation, individual O. longinoda were O. longinoda, Crematogaster spp. , Tetramorium observed carrying small beetles to its nest. It was spp. and fruit flies ( Bactrocera spp., Ceratitis observed that during immobilization, spp., Drosophilla melanogaster and Dacus spp.). aggressiveness of the prey led to the recruitment It was also observed that O. longinoda formed a of more members. In our observations, “chain” to transport food to other colonies of the the process of O. longinoda predation same species on different trees confirming involved attack, immobilization and transportation findings from Van Mele [19] who earlier reported of the prey to their nest. In one instance that O. longinoda preferred trees with closed observed in the coastal savannah zone, it took canopies and suggested that to improve their O. longinoda 30 minutes to transport a prey effectiveness, ropes could be attached between (beetle) to the nest. Larvae of coccinellids trees containing ant nests of the same colony. (Fig. 17g) and lacewings (Fig. 17h) were During “chain” formation, individual O. longinoda observed preying on citrus aphids. This stretches the hind, middle and forelegs to hold predatory behaviour of the coccinellids and each other. They also use the mandibles to hold lacewings reduced the population of aphids, the abdomen of the individual in front of them hence a reduction in the damage caused to the whilst members of the colony on adjacent trees citrus tree. Crematogaster spp. and Tetramorium

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spp. were also observed attacking adult insects vegetation of the understory of the citrus trees and Lepidopteran larvae in both agroecological (Fig. 18c). This observation contradicts the zones. findings of Dejean et al. [21] who reported that the nests of O. longinoda are always located in 3.6 Distribution of Nest of Some Insect tree canopies. Tetramorium spp. also built their Species in the Orchards nests using debris with the number of nests observed to be either one per tree or more. The The study showed that Crematogaster spp., nests were built under the citrus leaves with none Oecophylla spp., and Tetramorium spp. built their observed on the upper surface of the leaves nests in the citrus trees, however, depending on (Fig. 18d). the species, the nest could be found in the trunk, under the leaves or in the canopy of the citrus 3.7 Adaptations to Escape from Natural trees. It was observed that Crematogaster spp. Enemies and or to Catch Prey built their nest on the trunk/branch of the tree with sand or dead plant materials mixed with an Some insect species mimic the shape or oily substance produced by the larvae. The colour of the host plant making them less visible maximum number of nests built by to their natural enemies. Atlanticus gibbosus Crematogaster spp. (Fig. 18a) was two per citrus (Fig. 19a), Acrida conica (Fig. 19b) and tree but in most cases one per tree. O. longinoda Orophus sp. (Fig. 19c) were insects observed built its nest in the tree canopy by binding depicting various kinds of adaptations in the adjacent leaves together using silk produced by orchard during the study period. This behaviour the larvae. The nests of O. longinoda were was also observed in spiders and was used observed to range from 0-13 nests per tree as a predatory strategy to ambush and kill their (Fig. 18b). The nests were also found in the preys.

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Figs. (1). Antagonism of Phasmomyrmex aberrans and Oecophylla longinoda, (2a) Oecophylla with Bactrocera invadens, (2b) Oecophylla with Ceratitis ditissima, (3) Oecophylla , termites and spider on the same citrus tree, (4) Oecophylla tending Lepidosaphes beckii (citrus scale insects), (5a) Diopsis longicornis mating, (5b) Promachus sp. Mating, (5c) Sagra femorata mating, (5d) Lycus trabeatus mating, (6a) Z. variegatus nymph damage, (6b) Z. variegatus adult damage, (7a) Phyllocnitris citrella damage, (8a) Camponotus sp., feeding on a flower bud, (8b) Oecophylla feeding on a flower bud, (8c) Crematogaster sp. feeding on a flower bud, (8d) damage caused, (9) Lepidopteran larval damage (10a) Fruit fly damage symptom, (10b) Fruit fly larva in a citrus fruit, (11a) Wood borer damage, (11b) Wood borer larva, (12a) Termite damage (12b) Macrotermes sp. feeding inside a citrus branch, (13) Gummosis (14) Drosophilla feeding (15) Oecophylla chain formation, (16a) Promachus sp. preying on a dipteran, (16b), Promachus sp. preying on a Brachon sp., (16c) Promachus sp. preying on a spider, (17a) Oecophylla preying on a millipede, (17b) Oecophylla preying on a beetle, (17c) Oecophylla preying on a spider, (17d) Oecophylla preying on a termite, (17e) Oecophylla attacking Camponotus sp., (17f) Oecophylla carrying lepidopteran larva, (17g) Coccinelid larva preying on aphids,(17h) Lacewing larvae preying on aphids, (18a) Nest of Crematogaster, (18b) Nest of Oecophylla, (18c) Nest of Oecophylla in the undergrowth, (18d) Nest of Tetramorium sp., (19a) Atlanticus gibbosus leaf-mimicking, (19b) Acrida conica leaf- mimicking, (19c) Orophus sp. leaf-mimicking, (20a) Leptoglossus on a Passiflora fruit, (20b) Leptoglossus on a Passiflora leaf, (21a) Phoretic mites on a beetle, (21b) Phoretic mites on the ventral side of a beetle, (22) Phoretic mites on Zonocerus, (23) A beetle on a snail, (24a) A spider preying on flower visitors, (24b) Spiders preying on flower visitors, (25) Oecophylla trapped in a spider web, (26) A spider preying on a beetle larva

3.8 Other Observations on citrus fruits when the fruits matured. Phoretic mites such as citrus red mites Panonychus citri Leptoglossus spp. were commonly found in were observed on three separate occasions on a areas where Passiflora spp. were found beetle (Fig. 21a,b) and Z. variegatus (Fig. 22). A (Fig. 20a, b). They served as alternate host for beetle was also observed being carried by a snail Leptoglossus spp. in the orchards. It was (Fig. 23). On two different occasions, spiders observed that Leptoglossus spp. spent most of were observed hiding in citrus flowers, mimicking their time on Passiflora spp. and moved to feed the colour of the citrus flowers and making them

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inconspicuous to pollinators ambushing and research and the future of the citrus preying on the pollinators ultimately affecting industry in Ghana. Paper presented at the pollination services (Fig. 24a,b). Some spiders first Biennial National Agricultural were also found preying on Oecophylla (Fig. 25) Research Systems, Workshop; Accra, and beetles (Fig. 26) in the orchards. Insects Ghana. 1998;18. were found to be transporters of other pests such 3. Ceiba-Geigy Agrochemicals. The as mites in the orchards. Mites were found on mediterranean fruit fly Ceratitis capitata ; several occasions on the back of beetles and 1975. Zonocerus facilitating their dispersal in the 4. Morton J. Orange. In: Fruits of warm orchard. climates. Julia F. Morton, Miami, FL. 1987;134–142. 4. CONCLUSION 5. Afreh-Nuamah K. Importance of pests of citrus fruits in the Eastern Region of Our study showed that the interaction of insects, Ghana, Legon Agriculture Research spiders and mites could lead to either a reduction Bullettin. 1985;(1):27-43. or an increase in citrus production. Oecophylla 6. Ministry of Food and Agriculture MoFA. and Crematogaster driving away several insect Citrus production in Ghana. Horticulture pests such as Bactrocera , Ceratitis and Exports Industry Initiative (HEII). Crop Zonocerus could be used as biological control Services Directorate, Ministry of Food and agents against Bactrocera , Ceratitis , Zonocerus Agriculture. Agriculture information support and Macrotermes , however, Oecophylla and unit press. Accra, Ghana. 2007;108. Crematogaster could trigger an outbreak of 7. Ofosu-Budu KG. Performance of citrus sap-feeding insects such as the citrus scale rootstocks in the forest zone of Ghana. insects Lepidosaphes , citrus aphids ( Toxoptera Ghana Journal of Horticulture. 2003;3:1-9. aurantii,Toxoptera citricidus ) and citrus mealybug 8. Gullan PJ, Cranston PS. The insects: An Planococcus citri because they protect the sap- outline of entomology. Blackwell, Malden, feeders from their natural enemies. Spiders were Mass, USA; 2005. found to be predators of many insects in the 9. Gullan PJ. Cranston PS. Insects: An citrus orchards and were a threat to citrus fruit outline of entomology. Chapman and Hall; set as they hide in the citrus flowers and prey on 2010. flower visitors such as pollinators. Spiders also 10. Scholtz CH, Holm E. Insects of Southern preyed on Oecophylla which could affect Africa. Butterworths Professional biological control as well as integrated pest Publishers; 1989. management. Some species of ants fed on 11. Crowson RA. Coleoptera. Introduction and extrafloral nectar leading to the abortion of key to families. HIBI. 1956;4. flowers before fruit formation. The study showed 12. Ross HH. A textbook of entomology. that wild passion plant, Passiflora attracts and Topan Company Ltd. Tokyo. Japan; 1965. serves as an alternate host for Leptoglossus 13. McGavin GC. Insects, spiders and other which are pests of citrus. Citrus trees are terrestrial arthropods. Dorling Kindersley. susceptible to attacks by several insect pests 2002;255. including caterpillars of numerous lepidopterans, 14. Aidoo OF, Kyerematen R, Akotsen- citrus leaf miners, wood borers, termites, Mensah C, Afreh-Nuamah K. Effect of Zonocerus and ants. some climatic factors on insects associated with citrus agro- ecosystems in COMPETING INTERESTS Ghana. Journal of Biodiversity and Environmental Sciences. 2014;5(4):428- Authors have declared that no competing 436. interests exist. 15. Bawa AS. The study of the spatial distribution of some insects species in oil REFERENCES palm-cocoa intercrop. MPhil thesis, University of Ghana, Legon. 2009;61. 1. Adansi MA. Citrus stem-pitting virus at 16. Hill M, Holm K, Vel T, Shah NJ, Matyot P. Bunso, Ghana. Ghana Journal Agriculture Impact of the introduced yellow crazy ant Science. 1972;5:111-119. anoplolepisgracilipes on Bird Island, 2. Anno-Yarko FO. The major citrus Seychelles. Biodiversity and Conservation. production constraints; Status of citrus 2003;12:1969–1984.

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