effect of handling butterflies, which the butterflies probably perceived as a failed predation attempt. Heliconius are long-lived butterflies that repeatedly return to the same individual food and host-plants over a long period of time. Some species also maintain gregarious roosting sites, which they frequent every night (Gilbert 1975; Mallet 1986). Mallet et al. (1987) compared the percentage of individually recognized Heliconius butterflies that were re-sighted or re-captured at a given vine two days after the butterflies were either captured and marked, or just observed on the vine. Only 15% of the handled butterflies returned to the same vine two days later, compared with a 61% return rate two days after the observation alone. To eliminate the possibility of increased death rate of marked individuals, Mallet etal. also observed the butterflies at their roosting sites. They found that 30% of the handled butterflies and 13% of the observed butterflies did not return to the roosting sites on the same night of capture or observation, but that the proportions of non-returning butterflies converged after a few nights, with only 2% and 4% of the handled and observed butterflies, respectively, never returning to roost. These suggestive results invite carefully designed experiments using either butterflies or bees. An advantage of using honeybees for such study is the ability to mark bees upon emergence and later conduct long-term experiments, which include observations on the individually recognized foragers as they exit and enter the hive and at their foraging site (see Dukas & Visscher 1994).
Thomson (this volume) reviews evidence that, under some conditions, individual bumble bees visit individual plants repeatedly, in sequences termed traplines. If the bees can learn about specific routes and the rich patches along such routes, they can probably also learn to bypass hazardous locations (Craig 1994&).
In addition to modifying individual behavior, social bees may alter colony-level activity or the distribution of foragers. Korelov (1948, cited by Fry 1983) reported that flight activity near a honeybee hive was reduced from 90 to 4 bees per minute when bee-eaters preyed on bees at the hive entrance. It is feasible that honeybees, which recruit hive-mates to food-rich areas through dance (von Frisch 1967; Seeley 1996), quit recruitment when encountering predation near the hive, or reduce recruitment to a specific patch where they have experienced predation attempts.
Another way of responding to perceived predation risk is to modify foraging activity, such as reducing activity during riskier times. Another behavioral change may be to reduce meal size or the food load carried to the nest. In birds, increased body mass reduces maneuverability; birds are sensitive to this, as they maintain lower fat reserves under heightened predation risk (Metcalfe & Ure 1995; Veasey et al. 1998). Similarly, at least one insect study indicates strong effects of body mass on flight performance: Berrigan (1991) measured lift production in the flesh fly (Neobellieria bullata), finding that, compared to immature females, sexually mature females had 40% less lift than lighter immatures. Such decrease in flight performance can strongly decrease the fly's ability to escape from approaching predators.
The life span of worker honeybees decreased when weights were attached (Wolf & Schmid-Hempel 1989; Schmid-Hempel 1991). Although these studies focused on work load and physiological wear, increased predation due to decreased flight maneuverability may have contributed additional mortality.
If mass-dependent flight maneuverability is critical for successfully escaping predators, should flower-visiting animals stay lighter under heightened predation.? If predation occurs at flowers, perhaps decreasing the food load is the optimal strategy. However, if predation occurs predominantly during flight between the nest and flowers, the alternative of reducing the number of trips and increasing load per trip may result in higher fitness. This issue requires further evaluation.
Many bee species concentrate either in aggregations of solitary individuals or in social nests. Although foraging close to the nest may increase the net rate of food intake, the relative predation rate at flowers and on the way between the nest and flowers may alter the optimal patch distance (Dukas & Edelstein-Keshet 1998). For example, if most of the predation occurs during flight, bees should show a stronger preference for patches closer to their nest than predicted from energetic considerations alone. That is, in addition to floral traits, pollination levels and patterns of pollen flow are likely to be affected by the spatial distribution of colonial pollinators (most bees) and the patterns of predation (Dukas & Edelstein-Keshet 1998).
The timing of activity Predation risk typically varies among seasons and times of day, so pollinators may shift their activity season away from that of a major predator. For example, Schmid-Hempel et al. (1990) suggested that parasitoids were responsible, at least in part, for the very early activity period of some of the bumblebee species in their sites. These early-season bumble bee species escape the main activity season of the parasitoids, although the same seasonal pattern may be explained solely by resource competition with other sympatric bumble bee species. Similarly, Svensson et al. (1999) suggested that the dusk activity of winter moths in Scandinavia occurred at the time of lower predation risk (see also Andersson et al. 1998).
Flower specialization and flower constancy Predation risk may also vary among food plants and spatial locations. The reasons for such inter-host or location variance are that animals may escape predation while occupying locations that (1) are not searched by the predators, (2) are inaccessible to predators, or (3) diminish efficient predator search (Price et al. 1980). For example, Geitzenauer & Bernays (1996) examined predation by paper wasps (Polistes arizonensis) on tobacco budworms (Heliothis virescens) occurring on sunflower (Helianthus annuus) and groundcherry (Physalis pubescens). They found higher predation on sunflower, perhaps because the caterpillars were more conspicuous on sunflower (Fig. 11.4). Such results have two relevant implications for pollinator behavior. First, if generalist predators are more attracted to one plant species than another due to a greater ease ofcapturing herbivores, the pollinators of that plant may also incur higher predation rates than those ofthe other plant. Second, various floral characteristics may generate distinct attack and predation rates on pollinators on different flowers.
Indeed, Morse (1981) suggested differences in attack and predation rates by crab spiders on three sympatric flowers. Spiders on pasture rose (Rosa carolina) attacked visiting bumble bees two times more frequently than spiders on common milkweed and goldenrod (Solidago juncea), but the success rate of the spiders was more than four times lower on the rose than either milkweed or goldenrod. Honeybees in that study visited only milkweed and goldenrod. The spiders attacked them four times more often on milkweed than goldenrod, with success rates of 7% on milkweed and 0% on goldenrod (Fig. 11.5). Although highly suggestive, Morse's comparative data do not allow calculation of the predation rate per pollinator visiting each of the three flower species.
In two studies, pollinator specialization has been associated with increases in long- (Strickler 1979) and short-term (Laverty & Plowright
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