DOI: 10.1111/eea.12383 Active aggregation among sexes in bean flower thrips (Megalurothrips sjostedti)oncowpea(Vigna unguiculata)

Saliou Niassy1, Sunday Ekesi1, Nguya K. Maniania1, Benedict Orindi1, Gerald B. Moritz2, Willem J. de Kogel3 & Sevgan Subramanian1* 1International Centre of Insect Physiology and Ecology, PO Box 30772-00100, Nairobi, Kenya, 2Faculty of Natural Sciences I, Institute of Biology, Martin Luther University, Halle-Wittenberg, Domplatz 4, 06108 Halle (Saale), Germany, and 3Plant Research International, Wageningen UR, PO Box 16, 6700AA Wageningen, The Netherlands Accepted: 23 June 2015

Key words: aggregation behaviour, dispersion index, grain legumes, semiochemical, Thysanoptera, Thripidae, Fabaceae

Abstract Male sexual aggregations are a common territorial, mating-related or resource-based, behaviour observed in diverse organisms, including insects such as thrips. The influence of factors such as plant substrate, time of day, and geographic location on aggregation of thrips is uncertain, therefore we monitored the dispersion of male and female bean flower thrips (BFT), Megaluro- thrips sjostedti (Trybom) (Thysanoptera: Thripidae), on cowpea, Vigna unguiculata (L.) Walp. (Fabaceae), over three cowpea growth stages and across three cowpea-growing areas of Kenya. Our results indicated that for all the crop growth stages, the density of BFTs varied over the time of day, with higher densities at 10:00, 13:00, and 16:00 hours than at 07:00 hours. Thrips densities did not differ among blocks at the budding stage, but they did at peak flowering and podding stages. Dispersion indices suggested that both male and female BFTs were aggregated. Active male aggregation occurred only on green plant parts and it varied across blocks, crop stages, and locations. Similarly, active female aggregation was observed in peak flowering and podding stages. Such active aggregation indicates a semiochemical or behaviour-mediated aggregation. Identification of such a semiochemical may offer new opportunities for refining monitoring and management strategies for BFT on cowpea, the most important grain legume in sub-Saharan Africa.

on corollas of flowers (Kirk, 1985; Milne et al., 2002). Introduction Over the past 20 years, aggregation behaviour has Male aggregation is a common territorial and mating- gained interest among thrips biologists (Kirk & Hamil- related behaviour exhibited by avians, amphibians, ton, 2004; Hamilton et al., 2005), leading to the mammals, and insects (Fiske et al., 1998). Such identification of species-specific male-produced aggre- behaviour is typically classified as substrate-based, as gation pheromones (Hamilton et al., 2005; Zhang observed in cicadas, tephritids, drosophilids, etc. Aer- et al., 2011; Akella et al., 2014) and contact phero- ial-based aggregations are found among dipterans, mones (Olaniran et al., 2013). such as chironomids, culicids, simuliids, and The bean flower thrips (BFT), Megalurothrips sjostedti ephemeropterans (Shelly & Whittier, 1997). Substrate- Trybom (Thysanoptera: Thripidae), is a key pest of grain based aggregation behaviour of male thrips has been legumes – especially cowpea, Vigna unguiculata (L.) Walp. reported widely (Kirk, 1985; Olaniran & Kirk, 2012). (Fabaceae) – in sub-Saharan Africa (Tamo et al., 1993; Males of the genera Thrips and Frankliniella aggregate Abate & Ampofo, 1996). It causes abscission of cowpea flowers resulting in significant yield losses of between 20 and 100% (Singh & Allen, 1980). The BFT also attack a * Correspondence: Sevgan Subramanian, International Centre of wide range of alternative hosts mainly in the pea family Insect Physiology and Ecology, PO Box 30772-00100, Nairobi, Kenya. E-mail: [email protected] (Fabaceae) (Tamo et al., 2002).

© 2015 The Netherlands Entomological Society Entomologia Experimentalis et Applicata 158: 17–24, 2016 17 This is an open access article under the terms of the Creative Commons Attribution-NonCommercial-NoDerivs License, which permits use and distribution in any medium, provided the original work is properly cited, the use is non-commercial and no modifications or adaptations are made. 18 Niassy et al.

Ecological studies on population dynamics over seasons different cowpea plants separated by a minimal distance have revealed that the BFT numbers greatly increase dur- of 2 m and placed in separate glass vials containing ing specific crop growth stages, especially at flowering and 70% ethanol for further observation of thrips in the podding (Ezueh, 1981; Salifu & Hodgson, 1987; Nyasani laboratory. The sex of adult BFT emerging from flowers et al., 2013). However, prior to this study, in field surveys was identified and the total number of thrips per flower for thrips on grain legume crops such as dolichos, we was recorded. noted that BFT males were highly aggregated. Many doli- chos plants recorded very few or no males, whereas in very Assessment of bean flower thrips aggregation across cowpea-grown few dolichos plants high numbers of BFT males (some- locations in Kenya times up to 15 per plant) were observed (S. Subramanian, To understand the variation in aggregation of BFT across unpubl.). Based on this observation, we investigated the cowpea-grown locations, field observations were taken at aggregation pattern among sexes of BFT on cowpea and podding stage in three provinces of Kenya: Nairobi pro- assessed whether aggregation behaviour is active or passive vince (Kasarani: 01.222S, 036.897E, and 1 602 m a.s.l.), and whether it is influenced by location, time of the day, Eastern province (Matuu: 01.160S, 037.530E and 1248.1 crop growth stage, or plant part. ma.s.l.), and Nyanza (Mbita: 00.431S, 034.208E, and 1140.0 ma.s.l.). In Matuu and Mbita, cowpea farms at podding stage were selected for sampling based on obser- Materials and methods vations in the Nairobi field experiment. On each farm, Monitoring of male and female BFT densities on cowpea observations on whole plants and flowers were taken at the Variation in male and female BFT densities in relation same time and interval as described above. Four to nine to time of day and crop growth stage was studied on a replicated observations on 10–15 plants were taken cowpea farm at the International Centre of Insect Phys- depending on the farm size and density of BFT per plant. iology and Ecology (icipe) headquarters in Nairobi, Thrips counts in Matuu and Mbita were compared with Kenya. observations at the podding stage at Kasarani, Nairobi. Cowpea (var. Kakamega) was planted, after the land was ploughed, harrowed, and ridged. Planting was com- Statistical analysis pleted in March 2013 corresponding to the long rains Analyses were performed using R v. 3.1.0 (R Development season in Kenya. The farm (40 9 45 m) was divided Core Team, 2014) using R Commander v. 1.6-3 (Fox into four planting date blocks (10 9 10 m) separated et al., 2009) and Agricolae v. 1.1-4 packages (De-Mendi- by a corridor of 0.5 m. In each block, planting was buru, 2013). To study the predictive factors for the undertaken successively at 2-week intervals between number of BFTs, a negative binomial regression model May and June 2013 with intra- and inter-row spacing was fitted because we had overdispersed count data as of 0.25 and 0.45 m, respectively. Standard agronomic suggested by O’hara & Kotze (2010). The likelihood ratio practices were adopted (Dugje et al., 2009). Observa- (LR) test strongly suggested that the negative binomial tions in each block with different planting dates were model was more appropriate than the Poisson model (LR undertaken at three crop growth stages: budding (BD) test: P<0.0001). To start with, a full model including sex, (5 weeks after planting when mostly unopened buds block, stage, their interaction terms, and time of the day and few first flowers were seen), peak flowering (PF) was fitted. The dispersion parameter for this model was (8 weeks after planting when more than 90% of plants 1.154 indicating that the data were overdispersed, meaning were flowering), and podding stage (PS) (10 weeks after that the variability encountered in the data is not equal to planting when most of the plants had young pods with the mean, as with the Poisson distribution. The negative a few flowers). Within each crop growth stage, observa- binomial model was further fitted for each stage sepa- tions were taken on the number of male and female rately. BFT for four consecutive sampling days. On each sam- To study the thrips dispersion on plants and flowers, pling date, 25 randomly selected cowpea plants were two indices were calculated: (1) Lloyd’s index of patchiness sampled at 3-h intervals, from 07:00 to 16:00 hours (LIP) (Lloyd, 1967) defined as using the whole-plant tapping method. This involved  9 s2 x tapping the plants gently for 5 on white enamel tray LIP ¼ 1 þ ; (25 9 45 cm) kept right below. The number of thrips x2 which fell on the tray were quickly estimated (Pearsall & Myers, 2000). Further samples of 10–25 flower buds where s2 represents sample variance and x is the sample based on the availability were randomly collected from mean; and (2) variance-to-mean ratio (VMR). If LIP>1, Aggregation of bean flower thrips on cowpea 19 the population is considered aggregated and as LIP the distribution is considered regular. To test whether the increases, the degree of aggregation also increases. If distribution was significantly different from that of a LIP = 1, then distribution is considered random. If LIP<1, random population, a v2 test was performed for VMR

Figure 1 Mean ( SE) number of male and female Megalurothrips sjostedti (bean flower thrips, BFT) (A) per plant and (B) per flower, at four times of the day (07:00, 10:00, 13:00, and 16:00 hours) and three cowpea crop stages.

Table 1 Factors predictive for the presence of Megalurothrips sjostedti on cowpea plants at three crop stages, based on a negative binomial model

Budding Peak flowering Podding Factor RR (95% CI) P RR (95% CI) P RR (95% CI) P Time 07:00 1 1 1 10:00 2.27 (1.31–3.95) 0.0026 2.11 (1.48–3.05) 0.0001 1.69 (1.30–3.76) 0.0001 13:00 2.17 (1.24–3.83) 0.0047 1.80 (1.25–2.60) 0.0019 2.91 (2.25–2.72) <0.0001 16:00 3.02 (1.76–5.24) <0.0001 2.66 (1.87–3.80) <0.0001 2.09 (1.60–0.86) <0.0001 Sex Female 1 1 1 Male 4.12 (2.39–7.14) <0.0001 0.65 (0.43–0.98) 0.0410 0.61 (0.44–0.72) 0.0048 Block 11 1 1 21.15(0.63–2.09) 0.6400 0.63 (0.42–0.96) 0.0310 0.51 (0.36–1.71) 0.0001 30.98(0.53–1.81) 0.9600 0.84 (0.57–1.26) 0.4000 1.24 (0.90–2.01) 0.1900 40.76(0.41–1.43) 0.4000 0.71 (0.47–1.08) 0.1100 1.46 (1.06–1.75) 0.0190 Sex*block Female:block 1 1 1 1 Male:block 2 0.03 (0.01–0.08) <0.0001 0.52 (0.26–1.02) 0.0590 1.05 (0.63–0.97) 0.8600 Male:block 3 0.03 (0.01–0.08) <0.0001 0.60 (0.32–1.12) 0.1100 0.60 (0.37–0.73) 0.0380 Male:block 4 0.01 (0.002–0.06) <0.0001 0.24 (0.11–0.52) 0.0004 0.45 (0.27–0.001) 0.0012

RR, risk ratio; CI, confidence interval; P-values are based on Wald tests. 20 Niassy et al. using the expression   s2 s2 x2 ¼ ðv2Þ¼ ðN 1Þ; x x with (N 1) degrees of freedom, where N is the number of observations (Hurlbert, 1990). In situations with aggre- gation, the cause of aggregation was determined (i.e., whether it was active – behaviour-mediated – aggregation or passive, influenced more by environmental factors). In this regard, the criteria outlined by Arbous & Kerrick (1951) were used to estimate the mean ‘aggregation’ size k (Southwood & Henderson, 2000): k ¼ x t; 2k where k is the mean number of individuals in the aggregation for the probability level allocated to υ, xis the sample mean, k is the dispersion parameter obtained from the negative binomial model, and υ is a function with v2 distribution with 2k degrees of free- dom. In interpreting k, we note that k<2 indicates that aggregation is more due to an environmental effect and not to active behaviour of the insect, whereas k>2 is an indication that the cause of aggregation is due to either factor, but especially active processes by the thrips (Salifu & Hodgson, 1987; Verghese et al., 1988). Field data collected in Matuu and Mbita were sub- jected to similar analyses. We used v2 tests to differen- tiate the proportion of male and female BFTs at each time of the day, block, and plant stage. All tests were performed with a = 0.05.

Figure 2 Mean ( SE) number of male and female Results Megalurothrips sjostedti per plant (A) in the four planting blocks, (B) at the four observation times (07:00, 10:00, 13:00, and Density of male and female BFTon cowpea plants 16:00 hours), and (C) at the three cowpea crop growth stages. The mean number of male and female BFT by crop stages Difference between numbers of males and females was significant and time of the day are summarized in Figure 1A. As the in all instances (v2 test: P<0.05). sex-by-block-by-stage interaction term was significant in the full/initial model (LR test: P<0.0001), a negative bino- mial model was fit for each stage separately with time, podding stages, it was significantly less likely to get male sex, block, and sex-by-block in the model (Table 1). The thrips as compared to females (Figure 2C). results indicated that for all the stages, the sex-by-block interaction term was significant (P<0.0001), implying the Density of BFTon cowpea flowers densities of male and female BFT varied across the blocks Negative binomial model results indicated that the differ- (Figure 2A). After controlling for sex and blocks, time of ence in female densities per flower was not significant the day was significantly associated with the density of across block or time of day, whereas it differed across crop BFT at all the plant stages and significantly more insects stages: female density per flower was higher at peak flower- were collected at 10:00, 13:00, and 16:00 hours than at ing (mean SE = 0.3 0.1; Z = 2.3, P = 0.018) and 07:00 hours (Figure 2B). Also, after controlling for time podding (3.0 0.4; Z = 2.7, P = 0.006) than at budding and block, it was four times more likely to get a male than (0.1 0.0). At all observation times, males were mostly a female BFT at the budding stage. At the flowering and absent in flowers over the crop growth stages (Figure 1B). Aggregation of bean flower thrips on cowpea 21

Table 2 Crowding indices for male and female Megalurothrips sjostedti by crop stage and block

Males Females Crop stage Block LIP VMR v2 P k LIP VMR v2 P k d.f. Budding 1 8.9 17.81 1923.1 <0.0001 3.68 1.5 1.21 131.2 0.0640 – 108 2 0.2 0.95 102.0 0.6200 – 1.7 1.32 141.7 0.0140 1.81 107 3 8.4 1.36 136.4 0.0091 0.09 1.3 1.14 114.4 0.1500 – 100 4 0.5 0.99 101.0 0.5100 – 2.9 1.65 168.1 <0.0001 1.02 102 Peak flowering 1 4.5 3.60 360.0 <0.0001 1.62 1.4 1.48 147.7 0.0014 4.26 100 2 4.9 1.95 192.7 <0.0001 0.62 1.5 1.37 136.0 0.0080 2.73 99 3 6.6 3.12 309.4 <0.0001 0.90 1.6 1.57 154.9 0.0003 3.61 99 4 1.4 1.05 101.2 0.3400 – 1.9 1.66 159.5 0.0001 2.89 96 Podding 1 4.3 6.85 678.5 <0.0001 4.18 2.1 3.92 388.4 <0.0001 7.85 99 2 3.6 3.38 334.3 <0.0001 2.37 2.1 2.35 232.9 <0.0001 3.83 99 3 2.7 3.13 309.9 <0.0001 2.94 1.3 1.91 189.4 <0.0001 11.60 99 4 3.0 3.23 319.4 <0.0001 2.84 1.5 3.09 306.4 <0.0001 14.63 99

LIP, Lloyd’s index of patchiness; VMR, variance-to-mean ratio; k, estimated number of individuals in the aggregation.

Table 3 Dispersion indices of female Megalurothrips sjostedti on sexes (Z = 5.0, P<0.0001). Compared to Matuu, BFT cowpea flowers numbers per plant were higher in Mbita (Z = 3.5, P = 0.0004), but not in Nairobi (Z = 1.815, P = 0.070). Crop stages LIP VMR v2 d.f. P k Male numbers per plant were much higher in Mbita Budding 1.3 1 273.7 265 0.3000 _ (mean SE = 36.2 2.9; Z = 8.1, P<0.0001) than in Peak flowering 2.2 1.4 233.9 165 0.0003 1.4 Nairobi (1.3 0.1) or Matuu (0.4 0.1). Similarly, < Podding 1.8 3.3 492.3 149 0.0001 12.8 female numbers per plant were higher in Mbita (7.7 0.5; LIP, Lloyd’s index of patchiness; VMR, variance-to-mean ratio; Z = 8.9, P<0.0001) than in Nairobi (2.7 0.1) or Matuu k, estimated number of individuals in the aggregation. (3.3 0.2). Male BFT densities were lower than female densities in Matuu (Z = 14.2, P<0.0001) or Nairobi Aggregated dispersion of BFT on cowpea plants and flowers (Z = 9.17, P<0.0001). In Mbita, male BFT densities were Overall LIPs for male and female BFT were 10.9 and 2.8, higher than female densities (Z = 16.9, P<0.0001). respectively, and the respective VMR were 8.26 and 3.32. Dispersion indices indicated that in all the locations, VMRs for males and females were significantly greater both male and female LIPs were significantly higher than 1 than 1 (P<0.0001; Table 2). Among males, the LIP values (Table 4). Male LIPs were always higher than female LIPs. were >1 except for blocks 2 and 4 in the budding stage and In the field, the values of k for both male and female BFT block 4 in the peak flowering (Table 2). Similarly the were >2 in Mbita and Nairobi only. As earlier noted in VMR were also >1 except for blocks 2 and 4 in the budding Nairobi, although males were occasionally spotted on stage and block 4 in peak flowering stage. The VMR for green plant parts, they were mostly seen on the leaves females were also significantly >1, except for blocks 1 and (Figure 3A); flowers of cowpea were mostly populated 3 at the budding stage. In general, LIPs for males were with female BFT (Figure 3B). higher than for females (Table 2). On cowpea flowers, the > LIP for female BFTs was 1 at the peak flowering and pod- Discussion ding stages (Table 3). The analysis of the cause of male aggregation indicated Previous studies of M. sjostedti have revealed that at higher that k was >2 in block 1 at the budding stage and in all densities the adults are highly aggregated (Salifu & Hodg- blocks at podding. At flowering, k was <2 in all blocks. In son, 1987), which is suggestive of aggregation behaviour. female BFT, k was >2 at peak flowering and podding. In However, beyond this indication and to the best of our flowers, k was >2 only at podding (Tables 2 and 3). knowledge, no detailed studies on aggregation in sexes of BFT or on factors associated with such aggregated disper- Bean flower thrips densities on cowpea at different locations in Kenya sion are available in the literature. Female BFT occur in Overall, the density of BFT varied across the three loca- cowpea flowers in low numbers during the budding stage, tions (P<0.0001) and this variation differed between the but increased with the crop growth stage. Several authors 22 Niassy et al.

Table 4 Dispersion indices of male and female Megalurothrips sjostedti on cowpea at Matuu, Mbita, and Nairobi (Kenya)

Males Females Location LIP VMR v2 P k LIP VMR v2 P k d.f. Matuu 5.7 3.1 537.9 <0.0001 0.79 1.3 1.9 330.2 <0.0001 0.00 175 Mbita 2.9 70.9 21477.3 <0.0001 91.76 2 8.4 2555 <0.0001 23.25 303 Nairobi 3.8 4.55 1816.8 <0.0001 3.14 1.8 3.17 1264 <0.0001 7.28 399

LIP, Lloyd’s index of patchiness; VMR, variance-to-mean ratio; k, estimated number of individuals in the aggregation.

A We also found out that both male and female BFT infested the green plant parts of the cowpea crop, whereas flowers were only infested by females. The density of BFT on plants differed across blocks, crop growth stage, and time of day. Although both sexes presented aggregation patterns, males were more aggregated than females and aggregations were mainly observed on the green plant parts, especially the leaves. Similar aggregation of males on terminal leaves were also observed in Pezothrips kellyanus Bagnall (Mound & Jackman, 1998; Mound, 2004; Navarro-Campos, 2013). However, previous reports on male aggregation of other thrips species indicated that it takes place mainly on the corolla of flowers (Kirk, 1985; Terry & Dyreson, 1996). Frequent mating behaviour by B P. kellyanus on ripe citrus fruits has been reported to occur during the late afternoon around 17:00 hours (Webster et al., 2006). Generally, females were observed in flowers and their numbers significantly increased from budding to pod- ding stages. This could be for feeding or oviposition, as reported in BFT and other thrips (Childers & Achor, 1995; Gahukar, 2004). In addition to higher LIP values observed in both sexes, the mean ‘aggregation’ size k values were >2, indicating active aggregation of both male and female, as suggested by Salifu & Hodgson (1987) and Verghese et al. (1988). Our results also reveal that factors such as block, crop growth stage, and location could influence BFT aggregation behaviour. In Figure 3 Aggregation of male and female Megalurothrips sjostedti many thrips species, similar aggregations have been on cowpea at the podding stage. (A) Males (slender and light ascribed to the possibility of a semiochemical-mediated coloured) on a leaf, (B) females (robust and black) on a flower. interaction between the sexes (Mound & Jackman, 1998; Milne et al., 2002). Aggregation pheromones responsible have observed such increase in BFT population from the for such behaviour in thrips species such as Frankliniella initial infestation at the budding stage (macroscopic flower occidentalis (Pergande) (Kirk & Hamilton, 2004; Hamil- buds to anthesis) to full infestation at later flowering and ton et al., 2005), Frankliniella intonsa (Trybom) (Zhang podding phases (Ezueh, 1981; Salifu & Hodgson, 1987; et al., 2011), and Thrips palmi Karny (Akella et al., Salifu & Singh, 1987). Recently, Nyasani et al. (2013) also 2014) have been identified. The active aggregation observed that BFT population on French bean, Phaseolus observed in this study and recent report on the presence vulgaris L., was significantly lower before flowering than of male sternal glands associated with pheromone pro- after. Our observation concurs with their findings and duction in BFT (Krueger et al., 2015), underlines the provides additional information with regard to sex-speci- need to identify possible pheromones associated with fic differences in infestation of cowpea growth stages. BFT aggregations. Aggregation of bean flower thrips on cowpea 23

Sexual communication in a diverse array of phy- Akella SVS, Kirk WDJ, Lu Y-B, Murai T, Walters KFA & tophagous insects is strongly influenced by host plant Hamilton JGC (2014) Identification of the aggregation chemistry (Landolt & Phillips, 1997). The increase in pheromone of the melon thrips, Thrips palmi.PLoSONE BFT populations as determined by cowpea growth 9: e103315. stage, and the aggregation of males and females in Arbous AG & Kerrick JE (1951) Accident statistics and the concept of accident-proneness. Biometrics 7: 340–432. leaves and flowers suggest interactions between host Bottenberg H, Tamo M, Arodokoun DY, Jackai LEN, Singh BB & plant cues and pheromones which need to be Youm O (1997) Population dynamics and migration of cow- investigated. The densities of adult BFT varied with pea pest in northern Nigeria: implication for integrated pest time of day with more insects collected at 10:00, management. Advances in Cowpea Research (ed. by BB Singh, 13:00, and 16:00 hours than at 07:00 hours. This vari- RDR Mohan, KE Dashiell & LEN Jackai), pp. 271–284. IITA & ation could be attributed to variation in temperature JIRCAS, Ibadan, Nigeria. and time of the day, which also affect flower opening Childers CC & Achor DS (1995) Thrips feeding and oviposition and closing in the host plant (Ekesi et al., 1999; Ige injuries to economic plants, subsequent damage and host et al., 2011). responses to infestation. Thrips Biology and Management (ed. – Among the three cowpea-growing areas, higher num- by BL Parker, M Skinner & T Lewis), pp. 31 51. Springer, New bers of BFT, especially males with higher aggregation York, USA. De-Mendiburu F (2013) Agricolae: Statistical Procedures for indices, were observed at Mbita than at Nairobi or Matuu. Agricultural Research: R Package v. 1.1-8. Available at: http:// This difference could be ascribed to the lower altitude in CRAN.R-project.org/package=agricolae (accessed on January Mbita, with higher temperature and higher humidity 2014). (Murage et al., 2012), which are among the preferred Dugje IY, Omoigui LO, Ekeleme F, Kamara AY & Ajeigbe growth conditions for BFT and its host (Bottenberg et al., H (2009) Farmers’ Guide to Cowpea Production in West 1997; Ekesi et al., 1999). Africa. International Institute of Tropical Agriculture, Aggregation of sexes in BFT may be influenced by fac- Ibadan, Nigeria. tors including crop growth stage, time of day, and biogeo- Ekesi S, Maniania NK & Onu I (1999) Effects of temperature and graphical parameters. However, further research should photoperiod on development and oviposition of the legume focus on defining factors associated with this aggregation, flower thrips, Megalurothrips sjostedti. Entomologia Experi- – such as mating/defence behaviour (Terry & Dyreson, mentalis et Applicata 93: 145 155. Ezueh MI (1981) Nature and significance of preflowering damage 1996), role of male aggregation pheromones (Milne et al., by thrips to cowpea. Entomologia Experimentalis et Applicata 2002; Hamilton et al., 2005), and their interaction with 29: 305–312. plant growth stages (Sampson & Kirk, 2013). Defining the Fiske P, Rintamaki PT & Karvonen E (1998) Mating success in factors associated with the aggregation and identification lekking males: a meta-analysis. Behavioral Ecology and Socio- of such aggregation pheromones may aid in refining mon- biology 9: 328–338. itoring strategies for BFT and in appropriate timing of Fox J, Liviu A, Ash M, Boye T, Calca S et al. (2009) Rcmdr: R management interventions. Commander. 1.5-4. R Package. Available at: http://CRAN.R- project.org/package=Rcmdr (accessed on January 2014). Gahukar RT (2004) Bionomics and management of major thrips Acknowledgements species on agricultural crops in Africa. Outlook on Agriculture – This study was funded by the African Union through the 33: 191 199. Hamilton JGC, Hall DR & Kirk WDJ (2005) Identification of a African Union Research Grant Contract no: AURG/108/ male-produced aggregation pheromone in the western flower 2012. We acknowledge icipe (Duduville, Nairobi, Kenya) thrips Frankliniella occidentalis. Journal of Chemical Ecology and icipe-ITOC (Mbita, Kenya) for use of the laboratory 31: 1369–1379. and field facilities on the campuses for the conduct of this Hurlbert SH (1990) Spatial distribution of the montane unicorn. study. We gratefully acknowledge the support from the Oikos 58: 257–271. IPM Cluster at icipe as well as the Thrips IPM programme Ige OE, Olotuah OF & Akerele V (2011) Floral biology and polli- technicians. We also acknowledge the editing assistance nation ecology of cowpea (Vigna unguiculata L. Walp). Mod- offered by Mrs. Dolorosa Osogo. ern Applied Science 5: 74–82. Kirk WDJ (1985) Aggregation and mating of thrips in flowers of Calystegia sepium. Ecological Entomology 10: 433–440. References Kirk WDJ & Hamilton JGC (2004) Evidence for a male- produced sex pheromone in the western flower thrips Abate T & Ampofo JKO (1996) Insect pests of beans in Africa: Frankliniella occidentalis. Journal of Chemical Ecology 30: their ecology and management. Annual Review of Entomology 167–174. 41: 45–73. 24 Niassy et al.

Krueger S, Subramanian S, Niassy S & Moritz GB (2015) Sternal R Development Core Team (2014) R: A Language and Environ- gland structures in males of bean flower thrips, Megalurothrips ment for Statistical Computing. R Foundation for Statistical sjostedti, and Poinsettia thrips, Echinothrips americanus,in Computing, Vienna, Austria. comparison with those of western flower thrips, Frankliniella Salifu AB & Hodgson CJ (1987) Dispersion patterns and occidentalis (Thysanoptera: Thripidae). Arthropod Structure sequential sampling plans for Megalurothrips sjostedti and Development 44: 455–467. (Trybom) (Thysanoptera: Thripidae) in cowpeas. Bulletin of Landolt JP & Phillips WT (1997) Host plant influences on sex Entomological Research 77: 441–449. pheromone behaviour of phytophagous insects. Annual Salifu AB & Singh SR (1987) Evaluation of sampling methods for Review of Entomology 42: 371–391. Megalurothrips sjostedti (Trybom) (Thysanoptera: Thripidae) Lloyd M (1967) Mean crowding. Journal of Animal Ecology 36: on cowpea. Bulletin of Entomological Research 77: 451–456. 1–30. Sampson C & Kirk WDJ (2013) Can mass trapping reduce thrips Milne M, Walter GH & Milne JR (2002) Mating aggregations and damage and is it economically viable? Management of the Wes- mating success in the flower thrips, Frankliniella schultzei tern Flower Thrips in strawberry. PLoS ONE 8: e80787. (Thysanoptera: Thripidae), and a possible role for phero- Shelly ET & Whittier ST (1997) Lek behaviour in insects. The mones. Journal of Insect Behavior 15: 351–368. Evolution of Mating Systems in Insects and Arachnids (ed. by Mound LA (2004) Australian Thysanoptera – biological diversity CJ Choe & JB Crespi), pp. 273–293. Cambridge University and a diversity of studies. Australian Journal of Entomology Press, Cambridge, UK. 43: 248–257. Singh SR & Allen DJ (1980) Pests, diseases, resistance and protec- Mound LA & Jackman DJ (1998) Thrips in the economy and tion in cowpea. Advances in Legume Science (ed. by RJ Sum- ecology of Australia pest management – future challenges. merfield & AH Bunting), pp. 419–443. Royal Botanic Gardens, Sixth Australian Applied Entomological Research Conference Kew, UK. (ed. by MP Zalucki, RAI Drew & GG White), pp. 472–478. Southwood TRE & Henderson PA (2000) Ecological Methods, University of Queensland, St Lucia, QLD, Australia. 3rd edn. Blackwell Science, Oxford, UK. Murage AW, Obare G, Chianu J, Amudavi DM, Midega Tamo M, Baumgaertner J & Gutierrez AP (1993) Analysis of the CAO et al. (2012) The effectiveness of dissemination path- cowpea agro-ecosystem in West Africa. II. Modelling the inter- ways on adoption of ‘push-pull’ technology in Western action between cowpea and the bean flower thrips Megaluro- Kenya. Quarterly Journal of International Agriculture 51: thrips sjostedti (Trybom) (Thysanoptera, Thripidae). 51–71. Ecological Modelling 70: 89–113. Navarro-Campos C (2013) Pezothrips kellyanus (Thysanoptera: Tamo M, Arodokoun DY, Zenz N, Yondo M, Agboton C & Thripidae), Nueva Plaga en Cıtricos; Comportamiento de Sus Adeoti R (2002) The importance of alternative host plants for Poblaciones, Muestreo y Enemigos Naturales. PhD Disserta- the biological control of two key cowpea insect pests, the pod tion, Universitat Politecnica de Valencia, Valencia, Spain. borer Maruca vitrata (Fabricius) and the flower thrips Mega- Nyasani JO, Meyhofer€ R, Subramanian S & Poehling H-M (2013) lurothrips sjostedti (Trybom). Challenges and Opportunities Seasonal abundance of western flower thrips and its natural for Enhancing Sustainable Cowpea Production (ed. by CA , enemies in different French bean agroecosystems in Kenya. Fatokun, SA Tarawali, BB Singh, PM Kormawa & M Tamo), Journal of Pest Science 86: 515–523. pp. 81–93. IITA, Ibadan, Nigeria. O’hara RB & Kotze DJ (2010) Do not log-transform count data. Terry LI & Dyreson E (1996) Behavior of Frankliniella occidentalis Methods in Ecology and Evolution 1: 118–122. (Thysanoptera: Thripidae) within aggregations, and morpho- Olaniran OA & Kirk WDJ (2012) Fighting behaviour of male metric correlates of fighting. Annals of the Entomological Soci- western flower thrips, Frankliniella occidentalis (Pergande). ety of America 89: 589–602. Acta Phytopathologica et Entomologica Hungarica 47: Verghese A, Tandon PL & Prasada Rao GS (1988) Ecological 125–132. studies relevant to the management of Thrips palmi Karny on Olaniran OA, Sudhakar AV, Drijfhout FP, Dublon IA, Hall DR mango in India. Tropical Pest Management 34: 55–58. et al. (2013) A male-predominant cuticular hydrocarbon, 7- Webster KW, Cooper P & Mound LA (2006) Studies on Kelly’s methyltricosane, is used as a contact pheromone in the western citrus thrips, Pezothrips kellyanus (Bagnall) (Thysanoptera: flower thrips Frankliniella occidentalis. Journal of Chemical Thripidae): sex attractants, host associations and country of Ecology 39: 559–568. origin. Australian Journal of Entomology 45: 67–74. Pearsall IA & Myers JH (2000) Evaluation of sampling methodo- Zhang P-J, Zhu X-Y & Lu Y-B (2011) Behavioural and chemical logy for determining the phenology, relative density, and dis- evidence of a male-produced aggregation pheromone in the persion of western flower thrips (Thysanoptera: Thripidae) in flower thrips Frankliniella intonsa. Physiological Entomology nectarine orchards. Journal of Economical Entomology 93: 36: 317–320. 494–502.