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Effect of Ant Attendance on Aphid Population Growth and Above Ground Biomass of the Aphid’S Host Plant

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Effect of Ant Attendance on Aphid Population Growth and Above Ground Biomass of the Aphid’S Host Plant EUROPEAN JOURNAL OF ENTOMOLOGYENTOMOLOGY ISSN (online): 1802-8829 Eur. J. Entomol. 114: 106–112, 2017 http://www.eje.cz doi: 10.14411/eje.2017.015 ORIGINAL ARTICLE Effect of ant attendance on aphid population growth and above ground biomass of the aphid’s host plant AFSANE HOSSEINI 1, MOJTABA HOSSEINI 1, *, NOBORU KATAYAMA 2 and MOHSEN MEHRPARVAR 3 1 Department of Plant Protection, College of Agriculture, Ferdowsi University of Mashhad, Mashhad, Iran; e-mails: [email protected], [email protected] 2 Kyoto University, Kyoto Center for Ecological Research, Japan; e-mail: [email protected] 3 Department of Biodiversity, Institute of Science and High Technology and Environmental Sciences, Graduate University of Advanced Technology, 7631133131 Kerman, Iran; e-mail: [email protected] Key words. Hemiptera, Aphididae, Hymenoptera, Formicidae, ant-aphid interaction, aphid performance, population growth, developmental stage, plant yield Abstract. Ant-aphid mutualism is considered to be a benefi cial association for the individuals concerned. The population and fi tness of aphids affected by ant attendance and the outcome of this relationship affects the host plant of the aphid. The main hypothesis of the current study is that ant tending decreases aphid developmental time and/or increases reproduction per capita, which seriously reduces host plant fi tness. The effect of attendance by the ant Tapinoma erraticum (Latreille, 1798) (Hymenoptera: Formicidae) on population growth and duration of different developmental stages of Aphis gossypii Glover (Hemiptera: Aphididae) were determined along with the consequences for the fi tness of the host plant of the aphid, Vicia faba L., in greenhouse conditions. The initial aphid density was manipulated in order to study aphid performance due to density-dependent changes in ant attend- ance. The population growth rate of ant attended aphids was more than that of unattended aphids. However, the ratio of 1st–2nd nymphs to adults in aphid populations attended by ants was lower. The yields of bean plants on which the aphids were attended by ants were signifi cantly greater than those of unattended plants. This study indicates that ants not only increase aphid fi tness in terms of their population growth rate, but also benefi t the host plant. INTRODUCTION can result in an increase in the abundance of the aphid and/ Mutualism is a reciprocal relationship in which all par- or in its per capita fi tness (El-Ziady & Kennedy, 1956; ticipants benefi t from the interaction (i.e., the profi ts ex- Bristow, 1984; Flatt & Weisser, 2000; Cooper et al., 2007; ceed the costs) (Fischer et al., 2002; Yoo & Holway, 2011; Yoo & Holway, 2011). Increases in the abundance and Yao, 2014). The cost to benefi t ratio in mutualism changes survivorship of aphids due to ant tending are reported by with the intrinsic features of both partners (e.g. the initial many authors (e.g. Flatt & Weisser, 2000; Renault et al., number of partners at the commencement of a relationship) 2005; Tokunaga & Suzuki, 2008). and biotic/abiotic environmental factors (Stadler & Dixon, From a general perspective on the nature of condition de- 1998; Styrsky & Eubanks, 2010; Yoo & Holway, 2011; pendency in mutualism, ant attendance not only has posi- Barton & Ives, 2014; Singh et al., 2016). Thus, mutualism tive effects (e.g. Breton & Addicott, 1992; Morales, 2000), has a context-dependent aspect, that is, the net benefi ts for but also negative effects on the per capita fi tness of aphids. a given species depend on ecological conditions (Zhang et Indeed, a reduction in body size and number of embryos in al., 2015). aphids (Stadler & Dixon, 1998; Yao, 2014) and predation The ant-aphid interaction is a common mutualism in upon aphids by ants (Pontin, 1958; Billick et al., 2007) are which ants provide aphids several benefi cial services, such reported costs associated with ant attendance. Given that as protection by removing the aphid’s natural enemies ant attendance can also infl uence the developmental time (Bronstein & Barbosa, 2002; Stadler & Dixon, 2005) and of aphid nymphs (Stadler & Dixon, 1998; Yao et al., 2000), reduce the incidence of disease by removing aphid waste examining its effect on aphids in each developmental stage products (i.e., honeydew) (Way, 1954; Yao et al., 2000) in can provide a critical insight into understanding the fi tness return for aphid honeydew. Consequently, ant attendance outcome and population dynamics of aphids (Cushman * Corresponding author; e-mail: [email protected]. Final formatted article © Institute of Entomology, Biology Centre, Czech Academy of Sciences, České Budějovice. An Open Access article distributed under the Creative Commons (CC-BY) license (http://creativecommons.org/licenses/by/4.0/). 106 Hosseini et al., Eur. J. Entomol. 114: 106–112, 2017 doi: 10.14411/eje.2017.015 et al., 1994). Although there is a substantial body of lit- condition as previously described for at least 4 generations before erature on the developmental time of aphids in life tables being used in this study. To prevent ants from accessing the aphid for ant attended and unattended aphids (Stadler & Dixon, colonies, each of the potted plants infested with an aphid colony 1998; Flatt & Weisser, 2000; Yoo & Holway, 2011), little is was placed in a tray fi lled with water. Colonies of the erratic ant, Tapinoma erraticum (Latreille, known about how ant attendance changes the age-structure 1798) (Hymenoptera: Formicidae), which is common in ag- of aphid populations. The primary objective of the present ricultural land in Mashhad and its surrounding area, were col- study is to determine how the population growth of the lected from several sites on the campus of Ferdowsi University aphid, Aphis gossypii Scopoli, is affected by the attend- of Mashhad, Mashhad, Khorasan-e-Razavi. The area from which ance of the ant, Tapinoma erraticum (Latreille, 1798) and they were collected is an open area with a dry climate and rela- how this is linked to changes in the age structure of the tively fertile soil covered by herbaceous plants. This species is aphid population. mainly reported to be from Iran’s northeastern region, specifi cally Since ant attendance might infl uence the developmen- the city of Mashhad (Hosseini et al., 2015). tal time of individual aphids and even the population dy- Fifty ant colonies, consisting of one queen and approximately 500 workers and a brood of 50, were prepared for this study. Each namics of aphids, it is necessary to determine how ant at- ant colony was kept in a Vaseline-lined polyethylene container, tendance changes during the course of aphid population which was half-fi lled with natural soil from an ant’s nest. The growth. Therefore, the present study’s second objective is container was placed in a tray fi lled with water to prevent the to determine how the level of ant attendance is affected by ants from escaping. It was partially covered with a dark piece of the size of an aphid colony. cardboard to maintain a dark environment, thus mimicking that As ant attendance may result in an increase in aphid pop- of a natural nest (henceforth, the container is referred to as an ulation size and aphid nymphs and adults ingest very large “ant nest”). The ant nests were placed in a greenhouse and ex- amounts of phloem sap, which can result in severe carbon posed to natural light condition. Before starting the experiments, and/or drought stress in the host plant (van Emden & Har- the ant colonies were fed for two weeks on a sugar solution (10 %)-fi lled glass tube (9 cm in height × 1.5 cm in diameter), which rington, 2007), the outcome of an ant aphid interaction can was loosely capped with cotton so as to allow the ants free access subsequently affect the growth or biomass of the aphid’s to the sugar solution. Water was sprayed twice a day onto the host plant. Hence, the third objective of this study is to surface of the soil in the ant nests to keep them moist. address whether ant attendance affects the growth (in this case, the above-ground plant biomass) of the host plant, Aphid population dynamics and age structure Vicia faba L. of the aphid by its effect on aphid colony size. To determine the effect of different initial aphid numbers on the intensity of the ant-aphid relationship and its effect on the MATERIALS AND METHODS above-ground biomass produced by the bean plants, a microcosm experiment was carried out in a greenhouse from September 3rd Plant, aphid and ant to October 25th, 2013. The experiment was of a completely rand- Vicia faba L. (Fabaceae, cv. Barkat) was used as the host plant omized design (3 × 2 full factorial) with three initial aphid num- of the aphid, A. gossypii, in this study. Vicia faba has extrafl o- bers (3, 12 and 24 aphids) with either ants present (AP) or not ral nectaries at the base of each leaf (EFNs), which are known present (non-AP). In this experiment, to determine how attend- to be attractive to ants (Katayama et al., 2014). The plants were ance by ants altered the developmental time of the different aphid individually grown from seed in 7-L polyethylene pots (23 cm stages and their reproduction, aphid developmental stages were in diameter × 17 cm in height) fi lled with a mixture of sand and recorded (see below). Each treatment combination was replicated clay (2 : 1). The pots were enclosed in transparent cylindrical fi ne- 5 times. Hence, 30 plants (at the 8–10 leaf stage) were used in this mesh cages (50 cm height × 30 cm diameter) and kept in a re- experiment. The plants were then placed inside of a rectangular- search greenhouse at the College of Agriculture of Ferdowsi Uni- shaped enclosure made of wood and covered with a gauze net versity of Mashhad, Mashhad, in northeastern Iran.
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