Are there significant levels of predation on pollinators

I watched these wasps at work all through that afternoon, and soon became absorbed in finding out exactly what was happening in this busy insect town. ... Now and then a wasp would fly out and, after half an hour or longer, return with a load, which was then dragged in. Every time I examined the prey, it was a Honeybee. No doubt they captured all these bees on the heath ... A rough calculation showed that ... on a sunny day like this several thousands bees fell victims to this large colony of killers. Tinbergen (1958, p. 21)

Niko Tinbergen's account of bee predation by the infamous bee-wolf, Philanthus triangulum Fabr., is just one of numerous anecdotal reports of apparently significant levels of predation on flower-visiting animals. I shall begin this section with a brief listing of the major predators of pollinators, proceed to review published data about predation on pollinators, and then evaluate the importance of predation, emphasizing its indirect effects on pollinators.

Major predators of flower-visiting animals

I shall focus here on predators that attack pollinators outside the nest, as these are most relevant to pollination ecology. I shall also include within my broadly defined "predator" category parasitoids that attack pollinators outside the nest. Parasitoids eventually kill their hosts, though there is some time delay between successful egg-laying and host death. Predation and parasitism inside nests, especially those of social insects, have been recently addressed elsewhere (Morse & Nowogrodzki 1990; Godfray 1994; Schmid-Hempel 1998). Outside the nest, predation on pollinators may occur at flower patches, where various ambush predators wait for flower-visiting insects, on the way between flower patches and the nest, or at the nest entrance. While some predators are confined mostly to one of the above locations, others are rather opportunistic.

The most frequent ambush predators that sit on or near flowers are crab spiders (Thomisidae) (Morse 1981, 1986), predaceous bugs (Hemiptera) (Balduf 1939; Greco & Kevan 1995), and praying mantids (Mantidae) (Canon 1990). Bee-wolves (Philanthus spp.) (Evans & O'Neill 1988) and other wasps (Evans & Eberhard 1970; De Jong 1990) commonly hunt for insects that are perching on flowers or flying near the colony. Orb-weaving spiders catch insects moving among plants (Robinson & Robinson 1970; Caron & Ross 1990). Pollinators are also attacked by robber flies (Lavigne 1992; Rabinovich & Corley 1997) and dragonflies (Fry

Many bird species are opportunistic predators of various pollinators. Among the more significant predators of bees are bee-eaters (Meropidae),

Old and New World flycatchers (Muscicapidae and Tyrannidae), swifts (Apodidae), swallows (Hirundinidae), shrikes (Laniidae), jacamars (Galbulidae), and drongos (Dicruridae) (Davies 1976; Fry 1983; Ambrose 1990). Nocturnal pollinators such as moths and hawkmoths are attacked by bats (Svensson et al., 1999). Various raptors are probably the most significant hummingbird predators, although information about hummingbird predation is scant (Miller & Gass 1985). Among parasitoids, conopid flies (Conopidae) are a major source of bumble bee mortality (Schmid-Hempel et al. 1990), and phorid flies (Phoridae) are known to attack honeybees in the New World tropics (Knutson & Murphy 1990).

Attack and predation rates on pollinators

Throughout this chapter, "attack" will mean an approach by a predator attempting to capture an individual. A successful attack results in predation, while an unsuccessful attack means that the potential prey escapes either harmlessly, or with some injury that may diminish fitness. Although there are numerous studies of predation on pollinators, only a few allow quantitative estimates of predation rates.

Morse (1979, 1981, 1986) presented detailed predation rates of crab spiders (Misumena vatia) on insect visitors to the common milkweed (Asclepias syriaca). In that study, a bumble bee (Bombus vagans) had a 14% chance of being attacked each day by a spider while visiting flowers. The daily attack probability for a honeybee (Apis mellifera) was 8%. The probability of predation per day was much smaller, 1.4% and 3% for a bumble bee and honeybee, respectively (Fig. 11.1).

Morse's estimates are much smaller than mortality rates of forager bumble bees and honeybees estimated from observations of foragers at observation hives. In such studies, the daily rates of non-returning workers range between 3% to 7% for bumble bees (Rodd et al. 1980; Goldblatt & Fell 1987) and 8% to 10% for honeybees (Wolf & Schmid-Hempel 1989; Dukas & Visscher 1994) (Fig. 11.1). On the one hand, Morse's data underestimate overall predation because they include only one predator. On the other hand, observations at the nest overestimate predation because worker disappearance may be caused by other factors, such as disorientation (Rodd et al. 1980).

Simonthomas & Simonthomas (1980) reported on the collapse of a local honeybee business at the Dakhla oasis in Egypt that was probably caused by high levels of predation by the bee-wolf, Philanthus triangulum. They cite similar cases in Western Europe. Philanthus triangulum is considered a

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