Effect of Interspecific Competition among Whiteflies (Homoptera: Aleyrodidae) on crops and ornamental plants in Southwestern Nigeria OYELADE, OJ

Whiteflies that are pests of many crops and ornamental plants produce migratory forms during dense populations with different species sharing the same host plant. Fields surveys of these pests were conducted from 8 sampling sites within the five states (Lagos, Oyo, Osun, Ekiti and Ondo states) of Southwestern Nigeria during 2016 and 2019 to investigate the effects of interspecific competition among whiteflies on plants in the region. This survey was carried out in both wet and dry seasons. Whiteflies were collected on crops and ornamental plants in the sampling sites within the mangrove forest, rainforest and the derived savannah zones in the region. Interspecific competition was observed between four species Aleurodicus dispersus, A cocois, Aleurocanthus woglumi and Bemisia tabaci. The species population of whiteflies was analyzed using the Paleontological statistics software package (PAST) and nonparametric t-test was conducted to analyse the sharing of the host surface among species. The results obtained showed that the interspecific competition among species of whiteflies in the region is most during early rain season and yielded less whiteflies infestation and abundance at underside of plant leaves, and as well supported high number of the pest on upper leaf surfaces. The integrative analysis of the consequences of interspecific competition could provide justification for predicting species exclusion resulting into whitefly invasions of upper leaf surfaces as their new ecological niche. DOI: https://dx.doi.org/10.4314/jasem.v24i12.24 Copyright: Copyright © 2020 Oyelade. This is an open access article distributed under the Creative Commons Attribution License (CCL), which permits unrestricted use, distribution, and reproduction in any medium, provided the original work is properly cited. Dates: Received: 01 October 2020; Revised: 20 November 2020; Accepted: 16 December 2020

Interspecific competition for space and food from host plants is often thought to be minor to play an important role in the structuring of most phytophagous insect population (Strong et al., 1984). The reason is that most season other factors like harsh climate, changing features of the host plant (morphology, allelochemistry, and nutrition), and natural enemies act in concert to maintain densities at levels well below those where interspecific competition has obvious impact ( Price 1983). Nevertheless, interspecific competition has been demonstrated for most insects and in particular for the sap-feeding Homoptera like whiteflies (Lawton and Strong 1981). Interspecific competition in whiteflies and other Homoptera can result in adverse effects on various fitness components and population growth, niche shifting (Salyk and Sullivan 1982), and competitive exclusion (McClure 1980 and. Whitefly species are worldwide pests of most vegetables, many agricultural crops and some ornaments especially in the sub-tropical and tropical regions around the world (Liu et al., 2007). The negative impact of the various whitefly species especially Bemisia tabaci (Gennadius) species complex had been severally reported to cause serious damage to their host plants through direct injury with their stylet insertion and by being a vector that transmit various viruses on their host plants (De Barro et al., 2011;Liu et al., 2013). Whiteflies are known for feeding on a wide range of different host plant families covering major plants like crops and ornamentals. They are host plant family specific in feeding habit but individual whitefly species often perform much better on some plant species (Powell and Bellows 1992;Oyelade and Ayansola 2015). This study probe into interspecific competition between four different whitefly species (Aleurodicus dispersus, A cocois, Aleurocanthus woglumi and Bemisia tabaci) that are present in all the ecological zones of Southwestern Nigeria during wet and dry seasons.

MATERIALS AND METHODS
Southwestern Nigeria is large, which is situated approximately between longitudes 002°49′ E and 006°20′ E of the Greenwich Meridian, and latitudes 06°00′ N and 08°50′ N of the Equator. Eight representative towns were selected within the five states-Lagos, Oyo, Osun, Ekiti and Ondo (Figure 1). Since the distribution of whiteflies is mainly influenced by the host plants and the factors affecting the host plants within their environment therefore, the selection of the study area in this research was based on the type of the vegetation in southwestern Nigeria (Mangrove, Rainforest and Derived Savannah). It was done in a way that towns with similar vegetation are not severally repeated. Random sample was made to represent the entire populations of Whiteflies present in the region. Sites with similar ecological pattern but different types of ornamental plants were repeated. The number of localities selected in Mangrove forest is lower than that of rainforest and derived savannah because of the homogeneity in the vegetation and ecological pattern in Mangrove forest. Sites representing various ecological zones and habitat types were sampled around Ibadan, Ado Ekiti, Ile-Ife , Idanre (rain forest); Ogbomoso, Igbo Ora and Ila Orangun (derived savannah) and Badagry (Mangrove forest). Black sooty mould deposited on the upper leaf surfaces on the field is the first striking feature signalling the presence of whitefly to the collector. However, sooty mould can also be produced by aphids, scale insects and mealy bugs. In order to ascertain that the sooty mould produced is from whitefly, collectors have to look out for whiteflies dense populations on the undersides of the leaves of host plant. Field collections of whiteflies were done by active and direct searching for adult insect and their various instars attached to the upper side of leaves. Puparia were attached to the leaves and collected directly by hands by detaching the leaf. The whole leaf with the puparia attached was detached and placed in a small envelope to be kept dry until required for preparation. Leaves with puparia attached were placed and stored in 95% ethanol prior to treatment. In identifying and describing whiteflies, morphological characters of the fourth instar (puparia) were used to separate the species. The taxonomic character of whiteflies is unlike other insects that use adult features for identification because whitefly identification is on immature form that is basically on their 4 th instar larvae (puparia). This study made use of existing Aleyrodidae taxonomic keys (Martin, 1987;Hodges and Evans 2005) for the identification of the four species under competition in the region. Data were analyzed with Paleontological statistics software package (PAST). Paired t-tests and analyses of variance (ANOVAs) plus post hoc pairwise comparison of the means were performed to determine whether populations were significantly affected by seasons and other species of whitefly present on the leaf surface.

RESULTS AND DISCUSSION
Aleurodicus cocois: The puparia has posterior two pairs of abdominal compound pores much smaller than remainder ( Figure 2) Submargin with numerous small wide-rimmed pores which are randomly arranged, this zone extending into subdorsum between the compound pores. Dorsal disc, mesad of compound pores, punctuated by scattered tiny Saturn-like pores ( Figure 3). Lingula with all 4 setae conspicuous.
Aleurodicus disperses: The pupal case vasiform orifice subcordate, wider than long (Figures 4 and 5). Compound pores are similar in size. Dorsal disc with a pattern of conspicuous septate pores in the submedian area, and much of subdorsal area with a dense pattern of wide-rimmed pores ( Figure 6). Bemisia tabaci: The pupal case is colourless to brown, deepening on the season and the position on the plant. Bemisia tabaci shows a great variation. This whitefly species is most easily recognized by the tubercles posterior to the vasiform orifice. Caudal setae always stout, usually at least as long as vasiform orifice (Figure 8). Vasiform orifice inset from margin of pupal case by less than its own length (vasiform orifice> caudal furrow), sided of orifice almost straight ( Figure 9).
Interactions between A dispersus versus A woglumi, B tabaci and A. cocois: A. dispersus infests at least 190 different plant species and showed preference to certain plant families (Oyelade and Ayansola 2015). The result of paired comparison of A dispersus with A woglumi, B tabaci and A cocois using non-parametric t-test was presented in Table 1. The comparisons between species were significantly different (P>0.05). This shows that A dispersus is always displaced to the upper side of the leaves by the presence of any of the other three species when they are in competition on plants. Individual species of any whitefly in southwestern Nigeria when solely occur on crop and ornamental plants stay underside of leaves but when they are found together on the same leaf at the same time in dense population, at least one of the four species will go to the leaf upper side surface. A dispersus is most common occurred on upper side of the plant leaves in southwestern Nigeria, follow by both A woglumi and B tabaci and then A cocois ( Figure 10). Nevertheless, if the whiteflies had first established on plants, adults were not attracted successfully on upperside plant leaves until competition with another species set in. Even adequate number of adults was not attracted on upper side, though adults showed preference to underside in most cases but when the competition between species intense on the same plant, the less privileged species results in moving to the upper side (Plates 1-4). This phenomenon reflects the behavioral attributes of adult whiteflies. Similar result was stated by Bird and Krüger (2006) where female B. tabaci adult stayed on the same host, and very few movements among host plants were recorded during their observation. It is also similar to the finddings of Omondi et al.(2005) who examined the host preference between two biotypes of B. tabaci namely cassava and okra biotype, where cassava biotype significantly chose cassava for oviposition and habitation rather than okra, Abelmoschus esculentus L. The host preference of competitive species in this study is also in accordance with the work of Shah and Liu (2013) who established whitefly populations on eggplant, tomato and cucumber where they found that host preferences were influenced by both whitefly populations and host plants however host plants played stronger role. Whitefly feeding can induce a defensive response on host plants to the other competing herbivores.  Interactions between A woglumi and B tabaci: A woglumi and B. tabaci exhibited similar feeding choice among different host plant families as well as leaf surfaces within a host ( Figure 11). The range of their host plants is not as wide as that of A dispersus but whenever they are found together on the same plant, A woglumi take advantage of its excessive secretion of honey dew and displace B tabaci to the upper side of the leaves. Table 2 showed that the competition between these two species is significantly different and when both found on single plant, A woglumi showed better performance for feeding host than that of B tabaci. Honeydew considered a nutrient rich substitute for the Hemipteran parasitoids. This finding is similar to a study that revealed host secreted honeydew as substitute nutrition increased egg quantity and adult longevity of parasitoids (Burger et al., 2004); whereas host feeding might facilitate parasitoids to continue the high quality hydropic egg production that is essential for natural environment. * indicates probabilities that are significantly different (P ≤ 0.05). Burger et al. (2005) observed that parasitoids can be acquired advantage and increased their oviposition rate through host feeding compared to honeydew feeding. This task might be relevant under circumstances of high host population density or high mortality of parasitoid adults and if other sources of food may not provide sufficient nutrition for egg production (Shah et. al., 2015). Interspecific competitive interactions act on the determining of the function and structure of ecological communities.

Population Dynamics of competitors during Rain and
Dry seasons: All four species of whitefly (A dispersus, A woglumi, B tabaci and A cocois) were found in all the ecozones in southwestern Nigeria (Table 3). Estimates of competition abundance indicated that A dispersus was maintained at a density one order of magnitude higher than that of A woglumi and B tabaci in all the seasons except in late rainy season ( Figure  12). Both A woglumi and B tabaci proliferated in parallel with each other in competition and occur only in late dry and early rain season (Table 3) but A woglumi then significantly increased during the production of honey dew and become significant to displace B tabaci to the upper leaf surfaces (Plate 4). This finding is in accordance with the work of 1984). A cocois density was lower than in any of the other three species (Figure 10) and it only occurred in early rain only (Table 3). A dispersus density start to increase from early dry and peaked in early rain before decline to enter late rain where excessive rainfall wash off the whitefly easily from leaf surfaces. A woglumi and B tabaci densities started building up in late dry season and peaked in early rain and then declined in late rain (Table 3).

Conclusion:
The whitefly establishment onto upper side of leaves is mainly considered by presence of two or more species of whiteflies feeding on the same host plant at a particular time. The competition is most during early rain season. A dispersus is most found on the upper surface of plant leaves in southwestern Nigeria. Moreover, presences of competitive species with type of season as abiotic factor play a fundamental role to adapt whitefly on upper side of host plant leaves.