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Featured Articles in This Month’s Animal Behaviour
Animal Behaviour 83 (2012) 869–870
Contents lists available at SciVerse ScienceDirect
Animal Behaviour journal homepage: www.elsevier.com/locate/anbehav
In Focus
Featured Articles in This Month’s Animal Behaviour
Hornet’s Response to Honeybee Signal An approaching predator often elicits a call or a display from its prey. A classic example is stotting by a gazelle pursued by a cheetah. As it runs away, the gazelle interrupts its forward movement with high jumps into the air. A display such as this could benefit the prey because it may reduce the probability of an attack by the predator. It could also benefit the predator, which may decide to approach another undisturbed and less vigorous individual. Such ‘I see you’ prey–predator signals can evolve only if the prey can back up its display with a reduced probability of success for the predator. For example, a stotting gazelle should stand a chance of outrunning a pursuing cheetah. This means prey–predator signals have to be honest. In other words, they need to have a true deterrent effect. Providing convincing empirical evidence for pursuit-deterrent signalling in animals is difficult. Experiments could test hypotheses about the behaviour of the prey by manipulating it, for example, with a dummy predator. The downside of such studies, however, is that they could not test hypotheses about the predator’s response. The display by honeybees when a hornet approaches their colony has great potential for experimental manipulation of the behaviour of both predator and prey. Painstakingly and meticulously, scientists have been collecting empirical evidence that this display is an ‘I see you’ signal. When a potential flying predator, and a hornet in particular, approaches the nest of the Asian hive bee, Apis cerana, guard bees at the entrance simultaneously vibrate their abdomens from side to side for a few seconds (Fig. 1). The result is both visually and acoustically striking because there is an overall shimmering effect accompanied by loud buzzing. The guard bees are more than capable of backing up this collective display with defensive action. Hornets ignore the shimmering wave of vibration and sound only at their peril! A hornet that lands at the hive entrance is killed by a combination of heat and suffocation within a dense ball formed around it by up to 500 bees. By contrast, Western hive bees, Apis mellifera, do not perform a shaking display; their heat balling involves fewer bees and reaches lower core temperatures. Their guards tend to approach hornets individually and are more vulnerable to predation. These differences provide an opportunity to test predictions of the hypothesis that the shaking display in Asian hive bees is an ‘I see you’ signal. In the present issue (pp. 879–882), Ken Tan (Chinese Academy of Science, China), Zhenwei Wang, Hua Li, Shuang Yang, Zongwen Hu (Yunnan Agricultural University, China), Gerald Kastberger (University of Graz, Austria) and Benjamin Oldroyd (University of Sydney,
Figure 1. A yellow hornet, Vespa simillima xanthoptera, approaching guards of the Asian honeybee, Apis cerana, in Japan. Photo: Masato Ono.
Australia) test the following predictions about the behaviour of the hornet predator. First, the shaking display should repel hornets and reduce predation. Second, hornets should be more likely to approach the species that does not produce the display and more successful at catching their foragers or guards. The authors also test hypotheses about the behaviour of the prey. The intensity of the display should increase with the proximity of the threat and the species that produces a shaking display should not respond to the approach of a nonthreatening species. Ten colonies of Asian hive bees and 10 colonies of Western hive bees were studied. The authors videorecorded the behaviour of the guard bees at the nest entrance of each colony in response to at least 10 visits by hornets. In a separate experiment with the 10 colonies of Asian hive bees, they conducted three trials each with a tethered live hornet and a tethered live butterfly with each colony. The butterflies were slightly larger than the hornets and had conspicuous yellow and black warning coloration. The tethered hornets or butterflies were held at each of 10, 20, 30, 40, 50, 60 and 70 cm distance from the nest entrance. The results suggest that the shaking display repels the predators. Despite the similar distance of first approach towards nests of either species, on average the free-flying hornets remained further from the nest entrances of colonies of the Asian hive bee, the species that produces the shaking display, than from the nest entrances of colonies of the Western hive bee, the species that does not produce the display. Furthermore, the predation rate of
0003-3472/$38.00 Ó 2012 The Association for the Study of Animal Behaviour. Published by Elsevier Ltd. All rights reserved. doi:10.1016/j.anbehav.2012.02.007
870
In Focus / Animal Behaviour 83 (2012) 869–870
the Asian honeybees was lower, despite the longer time that hornets spent hovering in front of their nest entrances. Hornets captured a Western honeybee in 40% of hoverings and an Asian honeybee in only 17%. The authors also found evidence that the intensity of the display by the prey increased with the proximity of the predator. The frequency of abdominal shaking by Asian honeybee guards increased in an S-shaped manner with decreasing distance of the tethered, live hornet from the nest. By contrast, the response of Asian honeybee guards to the tethered, live, nonthreatening butterfly was virtually nonexistent. There was evidence for it only at very close proximity and the frequency of shaking was 10 times lower than the response to the hornet. Overall, these results demonstrate strong evidence that the shaking display of Asian honeybees is a pursuit-deterrent signal to their hornet predators. The display is known to repel nonhornet intruders too, but this study strongly suggests that its primary function is to deter hornets. How guards recognize hornets is a question for future experiments. Other studies have demonstrated the mutual tuning of the so-called ‘Mexican wave’ displays of opennesting honeybee species, such as the giant honeybee, Apis dorsata, and the distance of an approaching hornet predator. Indeed, such collective responses represent ‘We see you’ signals and a challenge for the future is to understand the underlying mechanisms of recognizing and deterring a predator collectively. Ana Sendova-Franks Executive Editor
Leapfrogging in Lady Beetles Herbivores are expected to aggregate in habitats where their plant resources are optimal and to avoid habitats where their predators are most abundant. How then should the predators distribute themselves? Theory suggests that the best solution for predators is to aggregate where their prey’s plant resources are best, even though they as predators make no direct use of the plants. This strategy is termed ‘leapfrogging’ because the predator’s attention skips over the adjacent trophic level to concentrate on the one that is two levels down. Leapfrogging puts the herbivores in a bind, forcing them to trade abundance of their resource against density of their predator. Theory predicts that in such a situation the herbivores may still aggregate where their plant resources are best, but to a lesser degree than would hold in the absence of their predator. Experimental tests of these predictions have seldom been attempted, because of the difficulty of assembling a system in which both predator and herbivore are free to choose between patches of a plant resource that vary in quality. This difficulty has been overcome in a study reported in this issue (pp. 883–890) by Amanda C. Williams and Samuel M. Flaxman of the University of Colorado. Williams and Flaxman used a three trophic-level system in which seven-spotted lady beetles are the predator, pea aphids are the herbivore and tic beans are the plant resource (Fig. 2). The authors manipulated quality of the plant resource by application of a nonprotein amino acid, DL-b-aminobutyric acid or BABA, which increases plant defences against phloem-feeding insects, without producing direct toxic effects. In preliminary experiments, Williams and Flaxman showed that the intrinsic rate of increase of the aphids decreased markedly as the concentration of BABA applied to the soil around the plants increased from 0 to 25 to 50 mM. Williams and Flaxman then ran a series of habitat selection experiments in which only lady beetles, only aphids or both simultaneously were allowed to choose between four tic bean plants, one
Figure 2. A seven-spotted lady beetle consumes a pea aphid on a tic bean plant. Photo: Jeff Mitton.
of which was exposed to 50 mM BABA, two to 25 mM BABA and the fourth to 0 mM BABA. In one set of 20 replicates, 160 wingless aphids per replicate chose between four such plants in the absence of any predators. Initially, equal numbers of aphids were placed on each plant, but within days the aphids assorted themselves according to plant quality, with numbers highest on the 0 mM plants, intermediate on the 25 mM plants and lowest on the 50 mM plants. The first key result came from a second experiment, in which four lady beetles per replicate assorted themselves among four plants in the absence of any aphids. Predators without the prey showed the same habitat preferences as prey without predators, spending the most time on 0 mM plants, less time on 25 mM plants and the least time on 50 mM plants. This result confirms the basic leapfrogging prediction: the predators use their prey’s plant resources as a cue in habitat selection, even though they do not consume the plants themselves. In a third habitat selection experiment, aphids and lady beetles simultaneously chose between four tic bean plants of varying quality. In 30 replicates of this experiment, habitat preferences by both predator and prey were influenced by plant treatment in the familiar direction: 0 mM plants were most preferred and 50 mM plants least preferred. The second key result of the overall study is that aphid distribution was more uniform across plants in this experiment, with the predator present, than in the experiment without predators. In other words, in the presence of the predator the distribution of prey shifted towards greater use of the worst plants and less use of the best plants. Both predator and prey in this system appear to be behaving adaptively: it is adaptive for predators to use quality of the prey’s resource as a cue for selecting habitat, and it is adaptive for prey to trade abundance of the predator against resource quality. What remains unclear is the mechanism by which predators assess plant quality, and whether the ability to make such assessments is general across factors that affect quality of the prey’s resource and across predator–prey systems. Thus the generality of these results must be weighed in further research. William A. Searcy Executive Editor
Contents lists available at SciVerse ScienceDirect
Animal Behaviour journal homepage: www.elsevier.com/locate/anbehav
In Focus
Featured Articles in This Month’s Animal Behaviour
Hornet’s Response to Honeybee Signal An approaching predator often elicits a call or a display from its prey. A classic example is stotting by a gazelle pursued by a cheetah. As it runs away, the gazelle interrupts its forward movement with high jumps into the air. A display such as this could benefit the prey because it may reduce the probability of an attack by the predator. It could also benefit the predator, which may decide to approach another undisturbed and less vigorous individual. Such ‘I see you’ prey–predator signals can evolve only if the prey can back up its display with a reduced probability of success for the predator. For example, a stotting gazelle should stand a chance of outrunning a pursuing cheetah. This means prey–predator signals have to be honest. In other words, they need to have a true deterrent effect. Providing convincing empirical evidence for pursuit-deterrent signalling in animals is difficult. Experiments could test hypotheses about the behaviour of the prey by manipulating it, for example, with a dummy predator. The downside of such studies, however, is that they could not test hypotheses about the predator’s response. The display by honeybees when a hornet approaches their colony has great potential for experimental manipulation of the behaviour of both predator and prey. Painstakingly and meticulously, scientists have been collecting empirical evidence that this display is an ‘I see you’ signal. When a potential flying predator, and a hornet in particular, approaches the nest of the Asian hive bee, Apis cerana, guard bees at the entrance simultaneously vibrate their abdomens from side to side for a few seconds (Fig. 1). The result is both visually and acoustically striking because there is an overall shimmering effect accompanied by loud buzzing. The guard bees are more than capable of backing up this collective display with defensive action. Hornets ignore the shimmering wave of vibration and sound only at their peril! A hornet that lands at the hive entrance is killed by a combination of heat and suffocation within a dense ball formed around it by up to 500 bees. By contrast, Western hive bees, Apis mellifera, do not perform a shaking display; their heat balling involves fewer bees and reaches lower core temperatures. Their guards tend to approach hornets individually and are more vulnerable to predation. These differences provide an opportunity to test predictions of the hypothesis that the shaking display in Asian hive bees is an ‘I see you’ signal. In the present issue (pp. 879–882), Ken Tan (Chinese Academy of Science, China), Zhenwei Wang, Hua Li, Shuang Yang, Zongwen Hu (Yunnan Agricultural University, China), Gerald Kastberger (University of Graz, Austria) and Benjamin Oldroyd (University of Sydney,
Figure 1. A yellow hornet, Vespa simillima xanthoptera, approaching guards of the Asian honeybee, Apis cerana, in Japan. Photo: Masato Ono.
Australia) test the following predictions about the behaviour of the hornet predator. First, the shaking display should repel hornets and reduce predation. Second, hornets should be more likely to approach the species that does not produce the display and more successful at catching their foragers or guards. The authors also test hypotheses about the behaviour of the prey. The intensity of the display should increase with the proximity of the threat and the species that produces a shaking display should not respond to the approach of a nonthreatening species. Ten colonies of Asian hive bees and 10 colonies of Western hive bees were studied. The authors videorecorded the behaviour of the guard bees at the nest entrance of each colony in response to at least 10 visits by hornets. In a separate experiment with the 10 colonies of Asian hive bees, they conducted three trials each with a tethered live hornet and a tethered live butterfly with each colony. The butterflies were slightly larger than the hornets and had conspicuous yellow and black warning coloration. The tethered hornets or butterflies were held at each of 10, 20, 30, 40, 50, 60 and 70 cm distance from the nest entrance. The results suggest that the shaking display repels the predators. Despite the similar distance of first approach towards nests of either species, on average the free-flying hornets remained further from the nest entrances of colonies of the Asian hive bee, the species that produces the shaking display, than from the nest entrances of colonies of the Western hive bee, the species that does not produce the display. Furthermore, the predation rate of
0003-3472/$38.00 Ó 2012 The Association for the Study of Animal Behaviour. Published by Elsevier Ltd. All rights reserved. doi:10.1016/j.anbehav.2012.02.007
870
In Focus / Animal Behaviour 83 (2012) 869–870
the Asian honeybees was lower, despite the longer time that hornets spent hovering in front of their nest entrances. Hornets captured a Western honeybee in 40% of hoverings and an Asian honeybee in only 17%. The authors also found evidence that the intensity of the display by the prey increased with the proximity of the predator. The frequency of abdominal shaking by Asian honeybee guards increased in an S-shaped manner with decreasing distance of the tethered, live hornet from the nest. By contrast, the response of Asian honeybee guards to the tethered, live, nonthreatening butterfly was virtually nonexistent. There was evidence for it only at very close proximity and the frequency of shaking was 10 times lower than the response to the hornet. Overall, these results demonstrate strong evidence that the shaking display of Asian honeybees is a pursuit-deterrent signal to their hornet predators. The display is known to repel nonhornet intruders too, but this study strongly suggests that its primary function is to deter hornets. How guards recognize hornets is a question for future experiments. Other studies have demonstrated the mutual tuning of the so-called ‘Mexican wave’ displays of opennesting honeybee species, such as the giant honeybee, Apis dorsata, and the distance of an approaching hornet predator. Indeed, such collective responses represent ‘We see you’ signals and a challenge for the future is to understand the underlying mechanisms of recognizing and deterring a predator collectively. Ana Sendova-Franks Executive Editor
Leapfrogging in Lady Beetles Herbivores are expected to aggregate in habitats where their plant resources are optimal and to avoid habitats where their predators are most abundant. How then should the predators distribute themselves? Theory suggests that the best solution for predators is to aggregate where their prey’s plant resources are best, even though they as predators make no direct use of the plants. This strategy is termed ‘leapfrogging’ because the predator’s attention skips over the adjacent trophic level to concentrate on the one that is two levels down. Leapfrogging puts the herbivores in a bind, forcing them to trade abundance of their resource against density of their predator. Theory predicts that in such a situation the herbivores may still aggregate where their plant resources are best, but to a lesser degree than would hold in the absence of their predator. Experimental tests of these predictions have seldom been attempted, because of the difficulty of assembling a system in which both predator and herbivore are free to choose between patches of a plant resource that vary in quality. This difficulty has been overcome in a study reported in this issue (pp. 883–890) by Amanda C. Williams and Samuel M. Flaxman of the University of Colorado. Williams and Flaxman used a three trophic-level system in which seven-spotted lady beetles are the predator, pea aphids are the herbivore and tic beans are the plant resource (Fig. 2). The authors manipulated quality of the plant resource by application of a nonprotein amino acid, DL-b-aminobutyric acid or BABA, which increases plant defences against phloem-feeding insects, without producing direct toxic effects. In preliminary experiments, Williams and Flaxman showed that the intrinsic rate of increase of the aphids decreased markedly as the concentration of BABA applied to the soil around the plants increased from 0 to 25 to 50 mM. Williams and Flaxman then ran a series of habitat selection experiments in which only lady beetles, only aphids or both simultaneously were allowed to choose between four tic bean plants, one
Figure 2. A seven-spotted lady beetle consumes a pea aphid on a tic bean plant. Photo: Jeff Mitton.
of which was exposed to 50 mM BABA, two to 25 mM BABA and the fourth to 0 mM BABA. In one set of 20 replicates, 160 wingless aphids per replicate chose between four such plants in the absence of any predators. Initially, equal numbers of aphids were placed on each plant, but within days the aphids assorted themselves according to plant quality, with numbers highest on the 0 mM plants, intermediate on the 25 mM plants and lowest on the 50 mM plants. The first key result came from a second experiment, in which four lady beetles per replicate assorted themselves among four plants in the absence of any aphids. Predators without the prey showed the same habitat preferences as prey without predators, spending the most time on 0 mM plants, less time on 25 mM plants and the least time on 50 mM plants. This result confirms the basic leapfrogging prediction: the predators use their prey’s plant resources as a cue in habitat selection, even though they do not consume the plants themselves. In a third habitat selection experiment, aphids and lady beetles simultaneously chose between four tic bean plants of varying quality. In 30 replicates of this experiment, habitat preferences by both predator and prey were influenced by plant treatment in the familiar direction: 0 mM plants were most preferred and 50 mM plants least preferred. The second key result of the overall study is that aphid distribution was more uniform across plants in this experiment, with the predator present, than in the experiment without predators. In other words, in the presence of the predator the distribution of prey shifted towards greater use of the worst plants and less use of the best plants. Both predator and prey in this system appear to be behaving adaptively: it is adaptive for predators to use quality of the prey’s resource as a cue for selecting habitat, and it is adaptive for prey to trade abundance of the predator against resource quality. What remains unclear is the mechanism by which predators assess plant quality, and whether the ability to make such assessments is general across factors that affect quality of the prey’s resource and across predator–prey systems. Thus the generality of these results must be weighed in further research. William A. Searcy Executive Editor