Ecological Entomology (2021), 46, 33–40 DOI: 10.1111/een.12937 Foragers of the stingless bee Plebeia droryana inform nestmates about the direction, but not the distance to food sources TIANFEI PENG,1 JÉFERSON PEDROSA,2 JAQUELINE ETERNA BATISTA,2 FABIO S. NASCIMENTO2 , and CHRISTOPH GRÜTER1 ∗ 1Institute of Organismic and Molecular Evolutionary Biology, Johannes-Gutenberg University of Mainz, Mainz, Germany and 2Departamento de Biologia da Faculdade de Filosofia, Universidade de São Paulo, São Paulo, Brazil Abstract. 1. The tropical stingless bees have evolved intricate communication systems to recruit nestmates to food locations. Some species are able to accurately communicate the location of food, whereas others simply announce the presence of food in the environment. 2. Plebeia droryana is a tiny Neotropical stingless bee that, until recently, was thought to use a solitary foraging strategy, that is without the use of a recruitment communication system. However, recent research has indicated that P. droryana might be able to recruit nestmates to specific food source locations. 3. We tested this by studying whether foragers can guide nestmates in the direction and the distance of artificial feeders placed in the vicinity of the colony. We trained bees to a scented sucrose solution feeder at 10 m and placed different feeders either in different directions (experiment 1) or in different distances (experiment 2). We found that P. droryana directs newcomers in the right direction, but distance information does not seem to be communicated. 4. Moreover, we then tested whether newcomers use chemical and visual cues originating from nestmates foraging at the food source, but found no evidence for the use of these social cues provided by conspecifics. 5. The potential mechanism that P. droryana may use to orient recruits toward the food source, however, remains unknown and requires further study. Key words. local enhancement, recruitment, stingless bees. Introduction intranidal mechanisms. The waggle dance in honeybees is a striking intranidal communication mechanism that has been Social insects have evolved a remarkable diversity of commu- studied extensively (von Frisch, 1967; Gould, 1975; Dyer, 2002; nication mechanisms to guide nestmates to food locations (Wil- I’Anson Price et al., 2019). A dancing bee indicates the distance son, 1971; Hölldobler & Wilson, 1990; Jarau & Hrncir, 2009). and direction of food sources to its followers (von Frisch, 1967; These communication mechanisms allow colonies to allocate Dyer, 2002; Couvillon, 2012). At the same time, followers gain workers to food sources that are too large to be exploited by information about the odour of the food source, for example dur- an individual and, thereby, collect more food for the colony. ing trophallaxis (Gil & De Marco, 2005; Farina et al., 2005; Communication mechanisms can be divided into extranidal and Farina & Grüter, 2009). Extranidal communication mechanisms include the laying of pheromone trails (in many ants) or tandem Correspondence: Tianfei Peng, Institute of Organismic and Molecular running (Hölldobler & Wilson, 1990; Franklin, 2014; Czaczkes Evolutionary Biology, Johannes-Gutenberg University of Mainz, Mainz, et al., 2015). 55122, Germany. E-mail: [email protected] Stingless bees (Apidae, Meliponini) are a large group of euso- ∗Current address: School of Biological Sciences, University of Bris- cial hymenopterans that live in diverse tropical and subtropical tol, 24 Tyndall Avenue, BS8 1TQ Bristol, U.K. habitats (Roubik, 1989). Several hundred species exist that show © 2020 The Royal Entomological Society 33 34 Tianfei Peng et al. a great diversity in lifestyle and ecology. While most genera to their nestmates but the mechanism is still a mystery (Flaig play a crucial role as pollinators, a few species have evolved et al., 2016). Furthermore, there are species where foragers seem carnivorous or robbing lifestyles (Camargo & Roubik, 1991; to only use information about the direction of food sources, Barth et al., 2008; Grüter et al., 2016). Food source commu- without using accurate distance information (Jarau et al., 2000; nication mechanisms in stingless bees are diverse and seem to Nieh et al., 2000; Nieh, 2004; Aguilar et al., 2005). More gener- be species-specific, ranging from simply motivating nestmates ally, recruitment communication remains poorly understood in to leave the nest and search for food to the precise communica- most stingless bees. This, in turn, has hampered our understand- tion of the food source location by using pheromone trails. Some ing of how complex recruitment communication systems have species are more efficient at recruiting nestmates to food sources evolved in social bees and how foraging strategies are related to than honeybees (Lindauer & Kerr, 1960; Aguilar et al., 2005; the lifestyle of different species. Barth et al., 2008). In Plebeia droryana,asmall(∼3 mm long) species commonly Intranidal recruitment communication is well-known in sting- found in South America, foragers have been shown to produce less bees. Successful foragers of many species perform “zigzag” buzzing sounds to alert nestmates about the presence of a or “jostling” runs inside the nest (Lindauer & Kerr, 1958, food source, but Lindauer and Kerr (1958, 1960) found no 1960; Hrncir et al., 2000), which usually takes place close evidence for specific location communication in this species. to the nest entrance (Nieh, 1998; Hrncir, 2009). The jostling Peng et al. (2019), on the other hand, found that the number of P. runs appear to play an important role in activating poten- droryana foragers steadily increased over time at a high-quality tial foragers (Hrncir et al., 2000). For example in Melipona food source, suggesting that P. droryana foragers might provide seminigra, inactive foragers significantly increased their own nestmates with specific location information. The two studies jostling activity after they were jostled by a recruiting bee differed in both the number of colonies observed and the (Hrncir, 2009). During the jostling runs and during trophal- foraging distance tested. While Lindauer and Kerr (1958, 1960) laxis, buzzing sounds are generated with thoracic muscles (Kerr used only a single colony and a relatively large foraging distance et al., 1963; Esch et al., 1965; Nieh & Roubik, 1998; Aguilar for such a small bee, Peng et al. (2019) studied five colonies at a & Briceño, 2002; Nieh et al., 2003b), which may stimulate nearby food source (10 m). Since food source distance affects the vibrated receivers to initiate foraging (Hrncir et al., 2006, recruitment probability (Nieh et al., 2003a, 2004; Stangler 2008; Hrncir & Barth, 2014; Krausa et al., 2017). At the same et al., 2009), it is possible that foragers were not motivated to time, the information of quality and odour of a food source is recruit in Lindauer and Kerr (1958, 1960). Here, we studied if potentially shared inside the colony by performing trophallaxis P. droryana foragers can potentially provide direction and (Nieh et al., 2000; Aguilar et al., 2005; Jarau, 2009; Krausa distance information to nestmates. Since foragers of some et al., 2017). species are attracted by visual and chemical cues of conspecifics Extranidal recruitment communication can involve foragers at food sources, so-called local enhancement (Slaa et al., 2003; laying a scent trail when leaving a food source, as found Slaa & Hughes, 2009), we also explored if the presence of in Cephalotrigona, Scaptotrigona,andTrigona (Lindauer & nestmates or their footprints at food sources affects P. droryana Kerr, 1958, 1960; Nieh et al., 2003a, 2004; Jarau, 2009) or the forager allocation. deposition of a scent beacon near the food source, which can attract other foragers (Nieh, 1998; Hrncir et al., 2004; Jarau et al., 2004; Alavez-Rosas et al., 2017). Furthermore, for some Materials and methods species, it has been suggested that visual tracking of guiding Study species and field site flights performed by recruiting foragers from nest to food source explains location-specific recruitment (Lindauer & Kerr, 1960; We performed all experiments on the campus of the University Aguilar et al., 2005). Recruitment success could also be the of São Paulo in Ribeirão Preto, Brazil. This area has many result of a combination of these mechanisms (Barth et al., 2008). different stingless bee species (Cortopassi-Laurino et al., 2009), However, most stingless bees do not seem to use pheromone and Plebeia droryana is among the most common ones. Wild trails to recruit nestmates, which may be due to the relatively colonies nest in tree cavities or in cavities in the walls of small colony size of many species (Nieh, 2004) as the number of buildings. We used eight wild colonies for our experiments. Wild workers in small colonies is not sufficient to sustain the volatile colonies were at least 100 m from each other. To prevent bees pheromone trails (Beekman & Dussutour, 2009). In addition, for from other colonies to visit our feeders, we closed all the visible larger colonies, it could be easier to dominate a food source, colony entrances within a 10 m radius around the focal colonies. which makes using pheromone trails potentially more beneficial Data were collected in February and March 2019 on days with (Aguilar et al., 2005). Thus, strong competition might favour good foraging conditions. recruitment communication in species with large colonies but select against recruitment in species with the small colony or body sizes (Johnson
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