The predatory behavior of the Neotropical social wasp Polybia rejecta
Introduction
Foraging is the basis for the survival, development and reproduction of individual animals. It permits their populations to endure while impacting other species, as seen through pollination, seed dispersal, parasitism and, for predators, the regulation of prey populations (Schoener, 1987; Kramer, 2001). To reduce the costs of food acquisition, animals must adapt their foraging behavior to spatially and temporally dynamic environments while avoiding their predators, so that theoretical models have been developed where the premise is that an optimization process results from natural selection (i.e., the notion of optimal foraging) (MacArthur and Pianka, 1966, Pyke et al., 1977).
In the case of a solitary predator a foraging bout includes the elements (1) search, (2) detection, (3) assessment resulting in pursuing or abandoning prey, (4) pursuit leading to prey contact and attack, (5) handling that includes mastering the prey, its preparation and consumption, and (6) processing or digestion (Kramer, 2001). Animals maximize benefits and minimize costs through an optimal diet based partly on the size of prey (i.e., a function of the time necessary to master them, or “handling time”), the choice of optimal patches to forage, the allocation of time spent in these patches, and the patterns of movement (i.e., foragers increase the sinuosity of their path and decrease their speed in favorable patches, known as “intensive search”; a patch is abandoned when the density of prey decreases). Therefore, when foraging, predators need to make decisions based on perceived cues related to prey density, quality and defenses, resulting in choices where risks are perceived as well as the possibility for inter- and intraspecific kleptobiosis (notion of decision rules; Stephens and Krebs, 1986, Kramer, 2001, Darracq et al., 2016).
Central place foragers, such as birds during the breeding season that return to their nests to feed their offspring or eusocial insects that feed their kin (i.e., nestmates and the brood of the colony), need to use navigation and memory to return to the nest and then to favorable patches (Orians and Pearson, 1979, Schoener, 1979, Hölldobler and Wilson, 1994, Sutton et al., 2015). In eusocial insects, the foraging bouts of solitary hunters are composed of (1) an outward trip, (2) search, (3) mastering the prey, (4) loading, (5) a homeward trip and (6) unloading (Kramer 2001). Although it can occur, the consumption of the prey is no longer the main objective of the forager. “Social foragers” have, in addition, the ability to inform their nestmates of the location of favorable patches (e.g., recruitment trails in ants and the waggle dance in honeybees) (Hölldobler and Wilson, 1994; Beekman and Dussutour, 2009). Loading can be optimized by retrieving large prey or successively capturing several small prey and retrieving them all at one time. Alternatively, partial loading often occurs when recruiting nestmates is needed to rapidly deplete a food source. Moreover, the theory predicts that when the load affects the duration of the homeward trip, the optimal load size decreases with an increasing distance to the nest (Schoener, 1979, Kasuya, 1982, Wetterer, 1989).
Because most social wasps (e.g., Vespinae and Polistinae including the swarm-founding Epiponini) are generalist predators preying mostly on caterpillars and adult Diptera and so can be used as biological control agents (Raveret Richter, 2000, Donovan, 2003, Jeanne and Taylor, 2009, Bichara Filho et al., 2010, Santana et al., 2012) they constitute a good model for studying their predatory behavior. The foraging bouts of social wasps begin with a flight towards a potential prey habitat. Then, search flights are composed of highly irregular loops alternating with phases of inspection where individuals hover while oriented toward a visible resource (Raveret Richter and Jeanne, 1991, Collett, 1995, Jander, 1997, Stürzl et al., 2016). Although prey, particularly live, fast-moving insects, are mostly detected by sight, odors also play a role (Raveret Richter and Jeanne, 1985, Hendrichs et al., 1994, Raw, 1998, Jeanne and Taylor, 2009, Couto et al., 2014). The prey capture behavior of Polistes dominula foragers is composed of the following phases: approach (generally walking), antennation, attack and biting various parts of the prey, butchering (slicing away pieces of flesh) and balling up (preparation of a small chunk of flesh to be transported). Finally, the ball of flesh is taken to the nest (Brown et al., 2012). The foragers of some Epiponini do not malaxate their prey, but rather transport them virtually intact or cut off only the non-edible parts, such as the wings; others retrieve only the most profitable part (e.g., the thorax of adult insects with the wing muscles), and still others cut large prey into pieces which are retrieved during successive flights (Jeanne, 1972, Hunt et al., 1987, Raveret Richter, 2000, Raveret Richter and Jeanne, 1991, Gomes et al., 2007, Jeanne and Taylor, 2009, Dejean et al., 2010, Dejean et al., 2012, Polidori et al., 2013). Although foragers generally kill live prey by biting them, stinging, a facultative phase, is triggered when the prey struggle. This permits the wasps to economize their venom which is only used to master large and/or vigorous prey (Edwards, 1980, Olson, 2000).
Navigation using sunlight angles, visual landmarks in the environment and a cognitive map (Collett et al., 2016, Stürzl et al., 2016) permits the wasps to take a direct homeward path. Learning flights (i.e., the individuals back away from the goal in a series of arcs) occur just after leaving the nest and before leaving a large food resource, permitting the foragers to find them later (Zeil et al., 1996, Jander, 1997, Stürzl et al., 2016). Capable of 24-h recall, foragers can undertake a series of return trips (Moreyra et al., 2016).
When moving to a new nest site, the Epiponini recruit nestmates by laying scent trails (Jeanne, 1981, Jeanne, 1991, Francescato et al., 1993, Howard et al., 2002), but this mechanism has never been observed during food recruitment (see Jeanne and Taylor, 2009). Yet, in Polybia occidentalis, naïve individuals in the nest use food scent cues from the carbohydrates brought in by successful foragers to orient themselves to food resources (social facilitation; Jeanne and Taylor, 2009, Shettleworth, 2010). Furthermore, in the field, the presence of conspecifics at a site attracts the foragers of different polistine species (local enhancement or increased likelihood of visiting a place by virtue of observing others doing it) (Raveret Richter, 1990, Hrncir et al., 2007, Schueller et al., 2010, Shettleworth, 2010, Taylor et al., 2012, Schueller and Jeanne, 2012; for Vespinae, see Santoro et al., 2015). Also, group hunting, likely related to a form of recruitment, has been noted in the Epiponini, illustrating the possibility of cooperation and coordination (O’Donnell and Hunt, 2013). Yet, except for tandem flights possibly performed by Vespula germanica foragers (Lozada et al., 2016), these types of information signals do not direct recruited individuals from the nest to the specific location of a food resource.
We studied the predatory behavior of Polybia rejecta (Epiponini) aiming to determine (1) when the wasps forage, (2) if visual cues are used to detect prey by using decoys, (3) the size/weight range of selected prey, (4) the differences in capture behavior according to prey size, (5) the impact of the prey-predator weight ratio on handling time, and (6) experimental manipulations to test for social enhancement, a form of recruitment to food resources.
Section snippets
Study sites and experimental set up
This study was conducted at the Hydreco field station at Petit Saut, Sinnamary, French Guiana (5°03′39″ N; 53°02′36″ W) between 2009 (preliminary observations) and 2015. The climate is tropical moist, with 3500 mm of annual precipitation distributed over 280 days. There is a major drop in rainfall between July and November (dry season) and another shorter and more irregular dry period in March.
The study area, the outer western wall of the Hydreco laboratory, is situated ≈200 m downstream from the
Size range of the prey/Cafeteria experiments
The first P. rejecta foragers began to hunt at 6:30 both during preliminary observations and when we noted the range of size of the prey selected by these foragers.
While the length of the insects attracted varied from 2 mm to 88 mm, the P. rejecta foragers captured only 4–14-mm long individuals (Fig. 2). Observations in the field permitted us to note that these wasps mostly hunt small caterpillars, grasshoppers and flies (see also Bichara Filho et al., 2010 for Polybia sericea). So, P. rejecta
Acknowledgements
We are grateful to Andrea Yockey-Dejean for proofreading the manuscript. Financial support for this study was provided by an “Investissement d’Avenir” grants managed by the Agence Nationale de la Recherche (CEBA, ref. ANR-10-LABX-25-01). The authors declare that they have no conflict of interest.
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