Foraging at a safe distance: crab spider effects on pollinators

Ecological Entomology (2017), DOI: 10.1111/een.12406 Foraging at a safe distance: crab spider effects on pollinators S P E N C E R H U E Y and J A M E S C . N I E H Section of Ecology, Behavior, and Evolution, University of California San Diego, La Jolla, California, U.S.A. Abstract. 1. The ability of pollinating insects to discover and evade their predators can affect plant–pollinator mutualisms and have cascading ecosystem effects. Pollinators will avoid flowers with predators, but it is not clear how far away they will move to continue foraging. If these distances are relatively small, the impact of predators on the plant–pollinator mutualism may be lessened. The plant could continue to receive some pollination, and pollinators would reduce the time and energy needed to search for another patch. 2. A native crab spider, Xysticus elegans, was placed on one cluster in a small array of Baccharis pilularis inflorescence clusters, and the preferred short-range foraging distances of naturally visiting pollinators was determined. 3. Nearly all pollinator taxa (honey bees, wasps, other Hymenoptera, and non-bombyliid flies) spent less time foraging on the predator cluster. 4. The key result of this study is that inflorescences within 90 mm of the crab spider were avoided by visiting honey bees and wasps, which spent three- and 18-fold more time, respectively, foraging on more distant flower clusters. 5. Whether honey bees can use olfaction to detect spiders was then tested, and this study provides the first demonstration that honey bees will avoid crab spider odour alone at a food source. Key words. Crab spider, foraging, honey bee, olfaction, pollination, predation, public information. Introduction The ability of prey to detect and avoid predators plays a major role in structuring ecosystems, in part by altering the spatio-temporal distribution of prey within a landscape (Laundre et al., 2010; Wirsing et al., 2010). Prey decision-making is affected by information about predator location and should be tuned to allow prey to forage in a dangerous world (Krupa & Sih, 1998). For prey that are pollinators, such decisions have a broad importance, because pollination is a key ecosystem service (Fisher & Turner, 2008). Predators can disrupt the plant–pollinator mutualism by deterring pollinator visitation, resulting in reduced seed set (Suttle, 2003), fruit production (Dukas, 2005; Hanna et al., 2012) and fruit biomass (Antiqueira & Romero, 2016). However, in some cases, predators can attract pollinators and thereby increase seed weights (Welti et al., 2016) Correspondence: Spencer Huey, Section of Ecology, Behavior, and Evolution, University of California San Diego, La Jolla, California, U.S.A. E-mail: spencer.huey@gmail.com; James C. Nieh, Section of Ecology, Behavior, and Evolution, University of California San Diego, La Jolla, California, U.S.A. E-mail: jnieh@ucsd.edu © 2017 The Royal Entomological Society or increase the plant’s reproductive success (fruit and seed set) by deterring less effective pollinators (Gonzalvez et al., 2013). Thus, the ability of pollinators to detect predators and fine-tune where and for how long they forage has complex, cascading ecosystem effects (Knight et al., 2006). In general, predator presence decreases the rate of pollina- tor visitation (Elliott & Elliott, 1994; Dukas & Morse, 2003; Suttle, 2003; Dukas, 2005; Goncalves-Souza et al., 2008; Jones & Dornhaus, 2011) because insect pollinators usually avoid inflorescences occupied by predators (Romero et al., 2011; Antiqueira & Romero, 2016). For example, crab spiders (Thom- sidae) are common ambush predators that prey upon a wide vari- ety of insect pollinators (Lovell, 1915; Nentwig, 1986). Insect pollinators therefore decrease visitation when crab spiders are on inflorescences of milkweed (Dukas & Morse, 2003), slickspot peppergrass (Robertson & Maguire, 2005) or other plant species (Reader et al., 2006). Visitation rates are important because they influence the probability of pollination (Kearns & Inouye, 1993). In addition, the duration of pollinator visitation can be positively correlated with pollinia removal (Fishbein & Venable, 1996) and with increased pollen deposition on stigmas (Thomson, 1986).