Foraging behavior of an aphidophagous female JBiopest 10(2):154-162 (2017)

Diurnalhoverfly. foraging behavior of an aphidophagous in an insectary patch

Chandrima Emtia and Kazuro O hno* JBiopest 5(1): 1-6 ABSTRACT A series of foraging bouts of Episyrphus balteatus (DeGeer) females were observed and recorded throughout the day in (Phacelia tanacetifolia Bentham) patches. The dominant transitions of interplant movement, approaching and probing bouts were statistically more frequent in the morning than in the afternoon. In the morning, interplant movement of foragers was significantly longer and they were moving at higher places of phacelia patches. They approached and probed flowers considerably longer in morning compared to afternoon. A significant positive relationship between the number of open flowers in a patch and the patch residence time was observed in the morning. The proportion of females having swollen abdomen filled with phacelia pollen (68.2%) in the afternoon was significantly higher than that (31.82%) in the morning. In our study, E. balteatus females spent more time foraging in phacelia patches in morning compared to afternoon. Based on the results and by considering the dual resources requirements of a female hoverfly (flower foraging and searching for to lay eggs), we will discuss the effective diurnal foraging of E. balteatus females in phacelia patches.

Keywords: Conservation biological control (CBC), Episyrphus balteatus (DeGeer), Foraging behavior, Insectary plant, Phacelia tanacetifolia (Bentham).

Citation: Chandrima Emtia and Kazuro Ohno. 2017. Diurnal foraging behavior of an aphidophagous hoverfly in an insectary plant patch. Journal of Biopesticides, 10 (2): 154-162.

INTRODUCTION (Tenhumberg and Poehling, 1995). However, adult require flower resources for Agricultural landscapes have been simplified their survival and reproduction (Hogg et al., at such a level that they no longer provide 2011; van Rijn et al., 2013; Van Rijn and natural enemies with appropriate resources in Wäckers, 2016). Several time and space, resulting in the development which are experimentally evaluated as of habitat management practices (Landis et al., insectary have great potential to 2000). One of the habitat management increase the adult hoverflies fitness. For practices is the provision of flower resources instance, phacelia (Phacelia tanacetifolia for enhancing conservation biological control Bentham) has been reported to enhance (CBC) of insect pests by predators and hoverfly, E. balteatus efficiency into parasitoids (e.g. White et al., 1995; Irvin et al., agricultural and horticultural systems as this 2006). For instance, aphidophagous hoverflies insectary plant increased its oviposition rate, larvae prey on aphids, while adults feed on lifetime fecundity and optimal reproductive flower resources such as pollen and nectar. potential (Laubertie et al., 2012). This Among the aphidophagous hoverflies, larvae insectary plant strips along winter wheat field of Episyrphus balteatus (DeGeer) (Diptera: margins were found to be effective in Syrphidae) has a great potential as a biocontrol enhancing E. balteatus population for agent of aphids (Chambers and Adams, 1986). controlling aphids (Hickman and Wratten, A single larva is able to feed on 660 to 1140 1996). Furthermore, Amorós-Jiménez et al. third-instar aphids during its development (2014) reported that the diet of adult hoverflies

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Emtia et al., influences performance of their larvae. 155 Moreover, aphidophagous females such as E. flowers. We planted this insectary plant in four balteatus need to select suitable colony such as plots of 3 x 2 m2 and one strip 1.0 x 10 m2 small and young colony consisting of nymphs from south to north edge of the field. Each of and or fundatrices as their oviposition sites for the plots and strip is termed as ‘patch’ in the the successful development of their offsprings present study. In the experimental field, (Kan, 1988). Therefore, the aphidophagous average temperature (°C) and relative female adults have to forage efficiently for humidity (%) were recorded to be 18.43 °C both flowers and aphids in a day. Hence and 70.5 % respectively by the thermo foraging decision such as allocating time recorder RTR-53 during the survey. budget for each of flower and resources Foraging bouts in the phacelia patches is vital for the aphidophagous hoverflies. The We observed the foraging behavior of E. time budget allocation can be governed by balteatus females following the focal sampling different extrinsic (e.g. time of the day, with continuous recording method adopted predation, physical structure of the from Martin and Bateson (2007). We surveyed environment, microclimate) and intrinsic the phacelia patches from 7am to 5 pm on factors (e.g. physiology, sensory and central sunny days using voice recorder and stop nervous capacities) (Kramer, 2001). The few watch to observe the foraging behavior of each studies which have been carried out on individual as it entered the patch and hoverflies foraging for flower resources were continued until it left. The behavior was based on the interaction between some of divided into foraging bouts which may be extrinsic and intrinsic factors of foraging termed as a period of time spending in behavior (Gilbert, 1985; Cowgill et al., 1993a; performing each of the foraging activities. We Cowgill et al., 1993b; Sutherland et al., 1999; followed each individual during their Pontin et al., 2006; Yokoi and Fujisaki, 2009). residence in each of the patch. Whether any of However, to the best of our knowledge, the the observed E. balteatus female re-entered in diurnal foraging pattern of female any of the phacelia patch was not considered aphidophagous hoverflies in insectary flower in the present investigation as it is not possible patches linking their dual resource to distinguish between each individual. The requirements (flower foraging and searching foraging bouts observed in phacelia patches for aphids to lay eggs) has not been studied in were as follows: interplant movement detail. The aim of the present study is to (including hovering), approaching, probing, evaluate the diurnal foraging behavior pattern landing on the flower, landing on leaf, of female E. balteatus in phacelia (P. grooming and flying out. Brief description of tanacetifolia) plant patches. Based on the these bouts are presented here. Interplant results, diurnal foraging activities of E. movement (including hovering) is the flight of balteatus in phacelia (P. tanacetifolia) plant E. balteatus from one plant to another phacelia patches are illustrated and the diurnal foraging plant in the patches. This bout includes pattern of E. balteatus females is discussed hovering which is a slightly motioned flight. considering their dual resource requirement. The pattern of interplant movement height of foraging E. balteatus in phacelia patches was MATERIAL AND METHODS determined by measuring the heights of 10 Study site, hoverfly and insectary plant The study of foraging behavior of this hoverfly phacelia plants from the ground level in each was conducted in an experimental field of 10 x patch. The measured height was used as a N & reference to estimate pattern of interplant ׳ m2 at University of Miyazaki (36° 14 10 E) from April to May, 2014. During movement height of E. balteatus. Approaching׳ 40 ° 59 this period, the predominant hoverfly was is the flight (hover) around <4cm of phacelia E.balteatus. The foraging behavior study of plants. Sometimes, they were touching the this hoverfly species took place during the flower corolla. Probing is the feeding on blooming period of Phacelia (P. tanacetifolia) pollen and nectar from the flower after landing

Foraging behavior of an aphidophagous female JBiopest 10(2):154-162 (2017) onhoverfly. the flower. We did not observe any nectar 156 feeding by the E. balteatus females in the E. balteatus becomes purple. Therefore, it was present study. These observation corroborate possible to use this purple colored abdomen as with the findings of White et al. (1995) in that an indicator of the abdomen condition of the theJBiopest deep corolla 5(1): 1 of-6 phacelia limits the nectar foragers. The abdomen status of E. balteatus accessibility to hoverflies. So this insectary was investigated by visually checking their plant was used as pollen source for abdomen, while they were foraging on the enhancement of hoverflies in their study. In phacelia plants in the morning and in the our study, the probing by E. balteatus females afternoon. The abdomen of the observed is considered as the pollen feeding of phacelia hoverflies was termed as swollen if purple flowers. Landing on the flower is the landing colored pollen filled the abdomen and flat of E.balteatus on the flower without probing when almost no pollen was present. it. Landing on leaf is a stationary activity. Statistical analysis Grooming is cleaning mouthparts or antennae Tests for normality of each group were and fly out is leaving of the patch. conducted using the Kolmogorov-Smirnov We recorded the duration of each of the test. The statistically significant difference of foraging bout. The sequence of each foraging the proportion of instances of the dominant bout was used to construct standard-style transitions of main foraging bouts in the transition matrices. Such a sequence is then morning and the afternoon was evaluated by summarized in a two-way frequency matrix, Chi-square test. Where the normality with the preceding activities in the rows and assumption was not met, the non-parametric the following activities in the columns Mann-Whitney U-test was used to compare followed after Van Der Heijden et.al., 1990. the duration of interplant movement, For example, if we can assume that different approaching and probing between morning activities can be distinguished then a and afternoon. Interplant movement height of frequency fij denotes the number of times that the foragers were checked by Kruskal-Wallis category i is followed by category j. These test followed by Dunn’s test for multiple frequencies fij can be collected into a matrix F comparisons. A Chi-square test was used to having I rows and I column. Thus we performed the statistical significant difference calculated the transition frequency for each of the proportion of individuals having flat and foraging bout sequences from the transition swollen abdomen between morning and matrices. afternoon during foraging. Moreover, linear Patch residence time regression analysis was performed to assess Patch residence time was calculated as the the relationship between patch residence time time between entering and leaving patch (i.e. of E. balteatus and flowering trend of phacelia cumulative duration of all the foraging bouts). in the patches. Kruskal- wallis test followed by To measure whether there is a relation Dunn’s test for multiple comparison test were between patch residence time of E. balteatus analyzed using Graph pad prism software, and available flower resource in the phacelia version 6 and all other statistical analyses were patch,a number of bearing open performed with SPSS software, version 19. flowers were counted by randomly selecting RESULTS AND DISCUSSION 10 plants per patch throughout the blooming Foraging bouts in the phacelia patches period of phacelia. Flower count was We observed the forging behavior of 126 and conducted in both morning and afternoon for 90 E. balteatus females in the morning and in every 3-5 days from the first week until the the afternoon in phacelia patches respectively. end of April, 2014. A total of 1709 sequences of the foraging Abdomen status of E. balteatus foraging in bouts in the morning and 1116 in the afternoon the phacelia patches of the foraging E. balteatus were observed. Upon feeding on the purple colored phacelia The matrices of transition sequences of the pollens in patches, the transparent abdomen of observed foraging bouts are given in Table 1

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Emtia et al., and Table 2 for the morning and the afternoon, 157 while the matrices of transition frequencies of probing duration of 25.556s in the morning these bout sequences are presented in Table 3 was significantly longer the than that of for the morning and the afternoon More than 15.204s in the afternoon (Mann-Whitney U- 70% of the transition sequences of the test, p< 0.05). foraging bouts were interplant movement to The females of Episyrphus balteatus were approaching, approaching to probing and observed moving from one phacelia plant to probing to approaching in both morning and another after entering the patch, and they afternoon (Table 1 and Table 2). Clearly, these approached flower resources during their flight transitions as well the foraging bouts included in phacelia patches. Therefore, we divided the were predominant in our study. The flying bout of E. balteatus in the phacelia probabilities of the dominant transitions of the patches into two foraging bouts namely, three main foraging bouts are presented in Fig. interplant movement and approaching. During 1 Transitions from interplant movement to the interplant movement in the phacelia approaching were significantly more frequent patches, perhaps, E. balteatus females were in the morning than in the afternoon (χ² = searching mainly for flowers which is also 7.892, p< 0.05). However, approaching to supported by our result that interplant probing transitions occurred less in the movement is transited in most of the cases to morning than in the afternoon (χ² = 15.931, p< approaching phacelia flowers by the foraging 0.05). Transitions from probing to the bout E. balteatus females (Table 1 and Table 2). conductive to continued feeding (approaching During approaching, E. balteatus females to floral resources) were greater in the might assess phacelia flowers, because, as the morning than in the afternoon (χ² = 8.295, p< results of transitions from approaching to 0.05). probing, interplant movement and landing on The mean interplant movement duration of flower during foraging by E. balteatus females 32.443s in the morning was significantly (Table 1 and Table 2) indicating that after longer than the mean interplant movement assessing the flowers through approaching, the duration of 16.163s in the afternoon (Mann- observed foragers probed on the rewarding Whitney U-test, p< 0.05; Fig.2). The heights flower; however, they transited to interplant of interplant movement varied significantly movement or landing on flower without with time in the morning and in the afternoon probing when the flowers were unrewarding. (Kruskal-Wallis test, p<0.05; Fig.3). In the foraging honey bees, approaching Considerably higher interplant movement was frequently led to probing of rewarding flowers observed between 8:00 and 9:00am and while this transition did not occur in the between 9:00 and 10:00am than at 14:00 until unrewarding flowers (Schmitt and Bertsch, 17:00 pm (Dunn’s multiple comparison test). 1990). Both interplant movement and The interplant movement height of E. approaching includes hovering so longer balteatus females from 8:00 until 11:00 am interplant movement and approaching flight in exceeded the average height of the phacelia the morning compared to that in the afternoon plants (47.3 cm), while their heights of indicated longer hovering in the morning. interplant movement were below the average Because, a typical feature of hoverflies flight height of the phacelia plants from 12:00 pm is hovering foralonger period of time until 17:00 pm in afternoon. The mean Syrphusrebesii is reported to be hovering 45% approaching duration was 3.466s in the of its flying time (Golding et al., 2001). This morning while in the afternoon it was 2.881s. slightly motioned flight is an energy expensive This bout was significantly longer in the flight (Kevan and Baker, 1973) which is morning than in the afternoon (Mann-Whitney utilized by the observed foragers for efficient U-test, p< 0.05; Fig. 4). The probing duration searching and assessing. This contention is of E. balteatus females in the morning and in simply supported by the argument that a the afternoon is shown in Fig. 5). The mean creature will not continue any costly activity if

Foraging behavior of an aphidophagous female JBiopest 10(2):154-162 (2017) it hoverfly.does not serve some advantage such as 158 increased efficiency e.g Norberg ( 1977) found females stayed longer in the morning in the that efficiency of searching strategy is linked phacelia patches. to energy expenditure Therefore, longer Fig. 1. The probabilities of the dominant interplantJBiopest movement5(1): 1-6 or prolonged searching transitions of the three dominant foraging and longer approaching or assessing of E. bouts of E. balteatus in the phacelia patches balteatus females in the morning compared to that in the afternoon (Figs. 2, 4) suggested that the observed foragers were searching and assessing actively for phacelia flowers in the morning in the phacelia patches. Foraging for flower seemed to be the most focused activity of E. balteatus females in the morning as along with longer searching and assessing, we also found longer probing of Fig. 2. Diurnal changes in the duration of phacelia flowers by E. balteatus females in interplant movement of E. balteatus in phacelia patches in the morning compared to phacelia patches that in the afternoon. This also corroborates with the finding of Gilbert (1985) in that among the observed diurnal foraging bouts, feeding (probing) was the longest for foraging E. balteatus in flower patches. For foraging hoverfly, Melanostoma fasciatum (Macquart), the focal foraging activity in flower patches is Fig. 3. Diurnal changes in the interplant probing (Pontin et.al., 2006). However, the movement height of E. balteatus in phacelia frequency of approaching to probing was flower patches lower in the morning compared to that in the afternoon and this may be explained by longer feeding which in turn caused lowered frequency resulting in the efficiency of foraging in the morning. The trade-off between the duration and the frequency of flower foraging was observed during nectar feeding by bumble bees (Jones et. al., 1998) Fig. 4. Diurnal changes in the duration of Nevertheless, more frequent transitions of the approaching of E. balteatus in phacelia observed foragers from probing to patches approaching (Tables 1 and Table 2) the in phacelia patches in morning compared to that in the afternoon which indicated an extensive feeding by the observed foragers because approaching in most of the cases lead to probing more frequently in the morning Figure 5. Diurnal changes in the duration of compared to in afternoon. The dominant probing of E. balteatus in phacelia patches. transitions and duration results of the major foraging bouts such as interplant movement, approaching and probing are clear indications that the observed foragers were more inclined in phacelia patches in the morning and subsequently, E. balteatus

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Patch residence time 159 The relationship between patch residence time movement height (Fig. 3) of these observed and the flower resources both in the morning foragers during foraging in the phacelia and in the afternoon are presented in Fig. 6. patches. Firstly, the abdomen condition of the The patch residence of E. balteatus was observed foragers revealed that most of the E. significantly positively correlated with balteatus females entered phacelia patches percentage of open flowers patch with flat abdomen in the morning while in the of phacelia in the morning (r = 0.541, p < afternoon they had swollen abdomen. This 0.05; Fig.6a). However, no such relationship result indicates that in the morning, E. was found in that in the afternoon (r = 0.149, p balteatus females were starved and as a result >0.05; Fig. 6b). The average patch residence these hungry foragers must stay longer in time was 7.6 min in the morning and in the phacelia patches to forage on the flowers more afternoon it was averaged 4.6 min. Generally, while in afternoon the observed foragers were flower foragers choose to stay longer in a already full fed and as a result stayed shorter patch of high density of flowers i.e. a patch for in the phacelia patches. Secondly, E. balteatus high reward. We found similar positive females might shift to other activity rather than relationship between flower density and patch flower foraging in the afternoon. This shifting residence of the observed foragers in the may be revealed by our foraging height result morning, while in the afternoon, such response that E. balteatus females were foraging in the was not found. patches at higher places in the morning and in Figure 6. Relationship between E. balteatus's lower regions in the afternoon in the phacelia patch residence time and percent of number of patches. Sutherland et.al. (2001) found E. open flowers in an inflorescence per patch of balteatus females in greater numbers in the phacelia. field margins where no flower resources were present, suggesting that they might be searching for aphids in the herbaceous host plants in those margins. The change in the interplant movement height between morning and afternoon might be suggesting shifting of foraging resources i.e. searching for phacelia flowers in the morning to aphid colony in the afternoon. In the foraging damselflies, the diurnal shift in the habitat utilization from searching for prey to reproduction has been reported by Hykel et al. (2017). Although it has already been reported that the matured hoverfly females need to travel between the flowering plants and crops to Abdomen status of E. balteatus foraging in forage for flowers and searching for aphids ( the phacelia patches VanRijn et al., 2006) , the diurnal behavior The abdomen condition of the foraging E. pattern of the females which need to forage for balteatus differed significantly (χ² = 9.82, p< the both resources have not been revealed. The 0.05) in themorning and in the afternoon. The present findings are the first to suggest that proportion of individuals having swollen there are variations in the diurnal behavior abdomen with phacelia pollen was 31.82% in pattern of E. balteatus females between morning while the 68.2% in the afternoon morning and afternoon in the phacelia patches. The difference in the foraging pattern of E. We could conclude from our study that aphid balteatus females between morning and ophagous female hoverfly, E. balteatus afternoon may be explained by our findings on foraged for phacelia flowers longer to the abdomen condition and the interplant maximize energy intake in the morning, while

Foraging behavior of an aphidophagous female JBiopest 10(2):154-162 (2017)

hoverfly.

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in the afternoon it spend less time in flowers ACKNOWLEDGEMENTS and in turn might spent time in activities We are grateful to the Ministry of Education, related to reproductive success i.e. one of the Culture, Sports, Science, and Technology of measured values of fitness which is supported Japan for granting a scholarship to CE by the argument that optimal utilization of (91206000630). time and energy of any forager is to continue REFERENCES any activity as long as the resulting gain in Amorós-jiménez, R., Pineda, A., Fereres A. time spent for per unit of food exceeds the and Marcos-garcía, M.Á. 2014: Feeding loss. This also fits with one of the assumption preferences of the aphidophagous of the optimal foraging theory that fitness of hoverfly Sphaerophoria rueppellii affect any forager heavily relies on its behavior the performance of its offspring. (Pyke, 1984). Nevertheless, as the BioControl, 59: 427-35. aphidophagous hoverflies forage for both Chambers, R. J. and Adams, T. H. L. 1986. resources in a day, our present findings have Quantification of the impact of hoverflies important implication in designing CBC of (Diptera: Syrphidae) on cereal aphids in aphids with hoverflies that we have to winter wheat: analysis of field emphasize on how to reduce the foraging costs populations. Journalof Applied Ecology, of the aphidophagous hoverflies for both 23: 895–904. flower sources and breeding site. Therefore, Cowgill, S. E., Wratten, S. D. and Sotherton, we suggest that insectary plants are required to N. W. 1993a. The selective use of floral be planted adjacent to the crop plants for good resources by the hoverfly Episyrphus control of aphids by hoverflies. balteatus (Diptera: Syrphidae) on

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