BEHAVIOR
Anticipatory and Reactive Crouching of Pea Aphids in Response to Environmental Perturbations MATAN BEN-ARI,1,2 STAV TALAL,3
AND
MOSHE INBAR1
Environ. Entomol. 43(5): 1319Ð1326 (2014); DOI: http://dx.doi.org/10.1603/EN14046
ABSTRACT Animals use different strategies to deal with changing environmental conditions. While standing and feeding on their host plant, aphids (Hemiptera: Aphididae) may be exposed to detrimental environmental perturbations, such as strong winds. If aphids are forcibly blown off the plant and spend time on the ground, they will face additional dangers by both ground-dwelling predators and detrimental soil temperature. It is therefore adaptive for aphids to behave in a way that lowers the risk of being removed from the plant. We observed that pea aphids (Acyrthosiphon pisum (Harris)) display a speciÞc crouched body posture, previously undescribed, which reduces their chance of being carried off from the plant by sudden winds. We exposed aphids in the laboratory to different cues indicative of a windy environment: wind, plant vibration, and visual stimuli. We found that aphids crouch in two situations: 1) reactively, when they are being pulled by a continuous gust of wind threatening to dislodge them. 2) Anticipatorily, when environmental cues, such as plant vibration or continuous movement near their host plant, may signify that sudden wind gusts are expected. Crouching aphids were less likely to be dislodged by a sudden air stream or plant vibration than were aphids that did not crouch. Crouching thus improves the aphidsÕ chances of remaining on their host plant under unfavorable environmental conditions. KEY WORDS Acyrthosiphon pisum, dropping response, environmental cue, incidental ingestion, wind
Many plant-dwelling insects spend most of their lives on various plant tissues, but they may be dislodged when natural enemies force them off the plant (Eisner and Aneshansley 2000) or when winds carry them off (Stork 1980). Once dislodged from the plant by winds, insects may be exposed to new, potentially detrimental abiotic conditions on the ground (e.g., AlonsoMejia and Arellano-Guillermo 1992) or ground-dwelling natural enemies (Losey and Denno 1998). To avoid these possible costs, insects and other invertebrates deal with winds in several ways. Some seek shelter in places that eliminate or reduce the effect of wind (Atkinson and Newbury 1984, Herberstein and Heiling 2001, Gish et al. 2011) and others hold on tightly to the substrate to avoid dislodgement (Duplouy and Hanski 2013). Insects have developed a variety of mechanisms to adhere to plant surfaces (Betz and Ko¨ lsch 2004) both at rest and when they are in danger of being dislodged. While there are many studies of the physiological (e.g., adhesive secretions) and morphological (e.g., special adhesive structures on tarsi) adaptations allowing insects to attach themselves to the surface (e.g., Eisner and Aneshansley 2000, Gorb and Gorb 1 Department of Evolutionary and Environmental Biology, University of Haifa, 199 Abba Hushi Av., Mt. Carmel, Haifa, 3498838, Israel. 2 Corresponding author, e-mail: [email protected]. 3 Department of Zoology, Tel-Aviv University, Ramat Aviv, TelAviv, 69978, Israel.
2002), few studies examined behavioral mechanisms that can reduce dislodgement. One such behavior is the altering of the insectÕs body posture to resist dislodgement. Surprisingly, even though the body posture of insects has been examined in a variety of contexts (e.g., Pearson and Rowell 1977, OÕNeill and Kemp 1992, Dejean 2011), few reports have associated this change in body posture with the attempt to withstand winds. In a rare example, Grace and Shipp (1988) found that grasshoppers assume a crouched body position and reduce their tendency to jump when wind speed increases. Aphids (Hemiptera: Aphididae) are small sap-sucking insects that might suffer dire consequences should they be forcibly removed from their host plant by winds. Aphids do not readily move from their feeding spot unless threatened or when feeding conditions on the plant deteriorate (Dill et al. 1990, Gish et al. 2010). Even when they do drop from their host plant, they reduce the chance of reaching the ground by holding on to lower leaves in the same plant (Ribak et al. 2013). The reason for this reluctance to drop is probably the various dangers that await aphids on the ground, including desiccation, ground-dwelling predators, and reduced feeding time (McAllister et al. 1990, Dill et al. 1990, Gish et al. 2012). While studying the escape behavior of pea aphids (Acyrthosiphon pisum (Harris)) (Ben-Ari and Inbar 2014), we noticed that some adult individuals that
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Fig. 1. An adult A. pisum on a fava bean leaf before (a) and during (b) a wind burst. During the wind stimulus the aphid is crouching, i.e., the abdominal side of the soma is pressed against the surface of the leaf and the antennae are lowered toward the aphidÕs back. (c) A schematic representation of the angles measured in the description of the crouching response: ␣, the angle between the body and the surface of the leaf; and , the angle between the antennae and the body. (d) The body-plant and body-antennae angles (means ⫾ SE) of crouching and noncrouching aphids. Asterisks denote statistically signiÞcant differences according to a StudentÕs t-test (P ⬍ 0.05, Ndisturbed ⫽ 12, Nundisturbed ⫽ 10).
were perched on plants that had been moved or experienced windy conditions displayed a unique, more crouched body posture. The abdominal side of these aphidsÕ soma was pressed against the surface of the leaf and the antennae were lowered toward the aphidÕs back (Fig. 1aÐ b). To the best of our knowledge, despite the extensive research done on aphid defense behaviors, such a crouching behavior and its adaptive value have never been mentioned in the literature. This crouching posture is not a general reaction to danger because aphids threatened by natural enemies or competitors display a variety of responses, including moving the antennae, recoiling, withdrawing the stylet, and even walking awayÑ but never crouching close to the plant (Dixon 1958; Dill et al. 1990; Stern
and Foster 1996; Hartbauer 2010; M.B.-A., unpublished data). In this study, we Þrst describe the crouching behavior and then address the following questions: A) What cues induce aphids to crouch? B) What is the adaptive value of this body posture? Does the crouched position reduce the chances of dislodgement from the plant? Materials and Methods Characterization of the Crouching Posture. Pea aphids were taken from a colony reared in the University of Haifa on Vicia faba L. broad bean plants in constant temperature of 20 Ð22⬚C, 50 Ð 60% relative humidity, and a photoperiod of 16:8 (L:D) h. In all ex-
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periments, we used only adult aphids, each used only once. To describe the crouching behavior, we placed aphids on the stem of a broad bean plant in a row (four aphids per plant), allowing us to photograph all aphids from the same plane, a left proÞle picture. We examined normally standing aphids after a 1 h rest (n ⫽ 10) and aphids that experienced environmental disturbance (n ⫽ 12). The plant of the disturbed group was lightly shaken by a single strike to the base of the plant using a plant-shaking device described by Ben-Ari and Inbar (2014). This device allows us to deliver a blow of repeatable strength with a carefully positioned rubber band. The photographs were enlarged on a computer screen to ease the measurements of the angle between the body axis and the plantÕs surface and the angle between the body axis and the third and fourth segments of the left antenna (see Fig. 1). The average angles of disturbed and undisturbed aphids were compared using a StudentÕs t-test. What Cues Cause Aphids to Crouch? We hypothesized that environmental stimuli that may dislodge aphids would induce the crouching response in aphids. In each of the following experiments, a colony of 10 Ð12 aphids was placed on a plant and allowed to settle for 2 h. Each type of stimulus was replicated 20 times. The treatments were arranged and mixed so that no complete set of replicates for a given treatment was performed in a single day. First, we tested whether aphids indeed crouched when exposed to wind that might dislodge them from the plant. We used a wind producing device (see details in Ben-Ari and Inbar 2014) to directly expose a group of 10 Ð12 aphids to a continuous airßow of 3.6 m/s from a 5 cm distance (the average wind speed measured in the spring over several days in an open Þeld in the Carmel Mt., when host plants are abundant and aphid colonies are at their peak). We noted the proportion of crouching aphids before the wind started, and then at 5, 30, 60, 120, 300, and 600 s. As even after 600 s (10 min) of continuous wind, most aphids were still crouched, we extended this examination. To test how long aphids would remain in this posture, we conducted a similar experiment in which we exposed the aphids to 60 min of continuous wind. It soon became clear that aphids crouch not only during wind bouts, but also minutes after the wind itself ceased. We tested whether aphids would also crouch when they encounter a short stimulus, one that could occur in a windy environment but does not persistently threaten to carry them off the plant. We used a short, 2-s wind gust from the wind producing device, and then examined the proportion of crouching aphids in the colony in the same times as in the continuous wind experiment. Plant vibration, which occurs because of the wind itself or because of blows from other moving plant parts, might also dislodge an aphid. We exposed the aphids to a vibration cue, using the aforementioned plant-shaking device that produces a single strike of repeatable magnitude to the base of the plant. We placed the device 2 cm above the base of the stem, waited 60 s to reduce any effect of the visual move-
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ment next to the plant (see Ben-Ari and Inbar 2014), and then applied the vibration. We examined the proportion of crouched aphids in the same aforementioned times. Both air movement and plant vibration are physical cues that might indeed dislodge an aphid. We tested whether detection of visual movement, which does not physically move the aphid but might be indicative of adverse conditions such as plant-parts moving in the wind or an approaching large predator, will also induce crouching in aphids. We exposed aphids to a visual stimulus without any air or plant movement. The visual cue consisted of a black rectangular object moving horizontally repeatedly from side to side on white background. This object was displayed on a 7.5 by 4.5 cm screen of a Samsung GT-S5620 mobile phone placed 5 cm from the aphid colony (as described in Ben-Ari and Inbar 2014). The screen was placed next to the aphid colony and the movie started after 60 s of a blank screen. The short visual cue consisted of the object moving from side to side for 2 s followed by a blank screen, and the continuous cue consisted of movement of the object throughout the treatment. Crouching proportions were noted in similar times as in the previous experiments. Because every aphid group was examined at each of the time intervals, the proportions of crouching aphids in a colony were statistically compared with a repeated-measures analysis of variance after arcsine of square-root transformation of proportion data with time interval as the repeated factor. When data were not normally distributed after transformation, they were compared using the corresponding nonparametric Friedman test. The Adaptive Significance of the Crouching Posture. To examine the possible adaptive value of crouching, we tested whether dropping from the plant while it is exposed to winds is more costly for aphids than dropping without winds because winds carry aphids away from the plant. When they drop to the ground, most aphids prefer to return to their host plant (Roitberg and Myers 1978, Gish and Inbar 2006) or catch on to lower leaves (Ribak et al. 2013). If winds carry the aphids away from the plant while they drop, it might be harder for them to locate a host. We placed 10 aphid colonies on 10-cm-tall fava bean plants (with the pot they were in, colonies were 20 cm off the surface of the table). We exposed the plants to winds of different velocities (0, 2.6, 3.6, and 4.6 m/s) and simultaneously induced the aphids to let go of their grip by using an apparatus emulating mammalian breath (as described in Gish et al. 2010, supplementary material), which causes many aphids to drop off their host plant. We examined the average horizontal distance of the dropping aphids from the base of the plant in each colony. This experiment was replicated eight times for each air-speed treatment (distances were averaged in each replication, so variability was reduced). As the variance of the data in the different groups was similar (according to LeveneÕs test), we performed a linear regression with wind velocity as the independent variable and distance of the landing
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Fig. 2. The proportion of crouching individuals (means ⫾ SE) from an aphid colony in response to a continuous gust of 3.6 m/s wind. In each bar N ⫽ 20 colonies of 10Ð12 aphids each. Control group was approached with the wind producing device but not subjected to wind. Every colony was examined at each of the times.
aphid from the base of the plant as the dependent variable. Crouching after an initial wind or vibration might also be adaptive if such a posture reduced the aphidsÕ chances of being dislodged by another sudden wind gust or plant vibration, for example, by improving their grip or reducing the windÕs drag on their bodies. To test this possibility, we examined whether aphids are able to reduce dislodgement by wind and plant vibration when they crouch. First, we tested whether noncrouching aphids might be dislodged by a powerful, sudden motion of air or of their host plant. We placed a single aphid on a fava bean plant and allowed it to rest for 2 h. We then exposed the aphids to one of two strong perturbations: 1) a stream of fast ßowing (8 m/s) air that was applied through a ßexible pipe held 5 cm from the aphid. 2) A strong vibration to the host plant, performed by pulling the rubber band in the plant vibration device to twice the usual distance. We examined the proportion of aphids that were dislodged by the wind or the strong vibration. We performed the same two treatments on aphids that were Þrst induced to crouch. Because preliminary results showed that the highest proportion of crouching was evident 60 Ð120 s after a vibration treatment, we induced crouching by applying an initial, regular vibration (that did not dislodge any aphid) and waiting 90 s before applying the strong vibration or wind gust. Every treatment was replicated 20 times, and the proportion of dislodged aphids was compared for each treatment (strong wind and strong vibration) between the crouching and noncrouching aphids using a Z-test for proportions. Results Characterization of the Crouching Response. After an environmental perturbation (gust of wind and plant vibration), aphids displayed a distinctive change in their body posture (Fig. 1aÐ b) in two main attri-
butes: They lowered their bodies and the angle between the body and the plant decreased threefold for crouching aphids (Fig. 1d, StudentÕs t-test; t ⫽ 4.498; df ⫽ 19; P ⬍ 0.001). The aphids also moved their antennae backwards and reduced the angle between the antennae and the body to nearly half of the angle in noncrouching aphids (StudentÕs t-test, t ⫽ 6.643; df ⫽ 18; P ⬍ 0.001). The Cues Inducing Aphids to Crouch. While before experiencing the cue aphids at rest hardly crouch (⬍10%), most of them crouched in response to a continuous wind gust pulling on their bodies and threatening to dislodge them. After 5 s of exposure to 3.6 m/s wind, most aphids (85Ð95%) were crouching and remained so even after 10 min of wind (Fig. 2). Only after an hour of continuous wind was there a decrease in the crouching proportion, with only 46.9 ⫾ 9.5% (mean ⫾ SD) of the aphids still crouching. Of the total aphids, 27.7 ⫾ 3% left the feeding place altogether to other locations on the plant or off the plant altogether. In the control group, which was not subjected to wind, only 3.3 ⫾ 1.4% of the aphids left the feeding place. The short cues elicited a different response (Fig. 3). After a 2-s wind gust or a vibration to the host plant, the aphids began to crouch, but not immediately. Only after 30 s did the proportion crouching gradually increase, reaching its peak 60 Ð120 s after the cue (79.9 ⫾ 3% in vibration cue and 70 ⫾ 3% in the wind cue). The proportion of crouching aphids then declined, returning to the initial levels 600 s after the cue. This change in crouching proportions was signiÞcant for both mechanical cues (wind: Friedman test, 2 ⫽ 109.373; df ⫽ 6; P ⬍ 0.001; vibration: Friedman test, 2 ⫽ 108.76; df ⫽ 6; P ⬍ 0.001). The aphids responded differently to the short and continuous visual cues (Fig. 4). While a short (2 s) visual cue did not induce crouching at all, as the visual disturbance continued, more and more aphids crouched, peaking at 60 s of continuous visual pertur-
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Fig. 3. The proportion of crouching individuals (means ⫾ SE) from an aphid colony in different time-lags after an initial short cue (2 s of 3.6 m/s wind or a single vibration to the base of the host plant). In each bar N ⫽ 20 colonies of 10Ð12 aphids each. The leftmost bar in both groups represents the proportion before the cue was applied.
bation (continuous visual: Friedman test, 2 ⫽ 109.105; df ⫽ 6; P ⬍ 0.001; short visual: Friedman test, 2 ⫽ 109.105; df ⫽ 6; P ⬍ 0.001). Afterwards, aphids slowly returned to a normal standing position. The Adaptive Value of Aphid Crouching. Strong winds caused dropping aphids to land further away from their host plant (Fig. 5), and thus most probably reduced their chances of returning to the same plant. Crouching aphids were far less likely to be dislodged (Fig. 6) by both a sudden gust of wind (Z-test for proportions, n1 ⫽ n2 ⫽ 20; Pcrouch ⫽ 0.25, Pnoncrouch ⫽ 0.85; Z ⫽ 3.814; P ⬍ 0.001) or by a strong vibration of their host plant (Z-test for proportions, n1 ⫽ n2 ⫽ 20; Pcrouch ⫽ 0.25, Pnoncrouch ⫽ 0.6; Z ⫽ 2.239; P ⫽ 0.025).
Discussion In this work, we described a new defense behavior of adult pea aphids: a crouching posture brought about by environmental cues. We found that by crouching pea aphids not only decrease the chance of being blown off a plant during a lengthy wind burst, but they also prepare for possible future bursts by changing their body posture in anticipation of possible future bursts. This anticipatory crouching posture allowed aphids to withstand sudden wind bursts and plant shaking and reduce the danger being dislodged by them. While we tested adult aphids, thirdÐfourth-instar nymphs perform this behavior as well (M.B.-A., unpublished data).
Fig. 4. The proportion of crouching individuals (means ⫾ SE) from an aphid colony in different times after a 2 s cue or during a long continuous visual cue. Each bar represents 20 colonies of 10Ð12 aphids each.
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Fig. 5. A linear regression of the distance of a dropping aphid from the basis of a 20 cm high plant as a dependent variable of the velocity of wind it was exposed to while dropping (P ⬍ 0.001).
Winds can affect aphids not only physically (by pulling on them and even dislodging them) but also physiologically. Winds can change the immediate physical environment of organisms and thus affect their water balance and thermoregulation (Kingslover and Watt 1983). Long exposure to wind may induce desiccation and cause stress and aphids dropped more readily in response to herbivore breath or even walked away from their feeding site after it was exposed to the prolonged wind bursts. Short wind bursts are less likely to desiccate an aphid but may affect its ability to remain on its host plant. Apterous aphids feed and stand on exposed plant parts and are therefore affected by sudden gusts of wind (Gish et al. 2011) and may be carried off the plant if they lose their grip. Many of the dropping aphids may return to their host plant (Calabrese and Sorensen 1978). Therefore, landing farther away from the host plant owing to winds could increase the time spent on the ground and substantially reduce the chances of an aphidÕs successful return. The main reason is that when traveling on the ground, aphids face the risk of predation, desiccation,
and loss of feeding time (Roitberg and Myers 1979, Gish et al. 2012). Hence, even when forced to drop, aphids attempt to grab plant parts on their way down to avoid reaching the ground (Ribak et al. 2013) and being carried away by wind, while dropping, will also reduce their chances of doing so. Crouching aphids are less likely to be dislodged by strong winds and plant vibration and can possibly reduce the chances of the unnecessary detrimental effects of time spent on the ground. Animals may behave in ways that do not necessarily match their current situation, but might be adaptive in the future (Correia et al. 2007). The behavioral mechanism that aphids use to counter dislodgement has at least two functions: reactive and anticipatory. Reactive responses are those that occur when a threat is present and evident and the response may lower the cost of this threat. Anticipatory behaviors are those that manifest without a threat present and reduce the possible costs should a threat appear suddenly (Cooper 1998). When aphids were exposed to a constant airßow, they reactively crouched and reduced the
Fig. 6. The proportion of aphids dislodged from the plant by a strong perturbation: sudden strong vibration or sudden strong wind burst. In each treatment N ⫽ 20. Crouching aphids are those that were subjected to a gentle vibration to the plant before the strong perturbation, inducing them to crouch.
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chances of being dislodged by the air pulling on their bodies, and indeed no aphid was blown off. The anticipatory reaction occurred when aphids detected a short cue indicating the chance of possible wind gusts in their environment, such as a short wind gust or plant vibration, and continued to crouch for some time. The anticipatory crouching did not start immediately after the short wind pulse or vibration cues, rather, its proportion increased during the Þrst 2 min after the cue. Cues such as plant vibration and air movement are somewhat unreliable, as they might arise not from winds but rather from a grazing mammalian herbivore approaching the aphidsÕ host plant (Ben-Ari and Inbar 2014). According to the latter study, in the Þrst few seconds after such cues, aphids are more inclined to drop from the plant, but after 30 s or more, as the unreliable cue is dissociated from mammalian presence and is interpreted as originating from winds, aphids are less likely to drop. The anticipatory crouching in this study shows the opposite trend from the tendency to drop from the plant reported in Ben-Ari and Inbar (2014). This contrast, higher crouching proportions coinciding with lower dropping tendencies, reinforces our interpretation that crouching aphids do so to lower the chances of being carried away by winds. Both modes of crouching (i.e., reactive and anticipatory) were very effective in dealing with the danger of dislodgement, but a sustained crouching posture may incur some cost. Though some insects crouch in preparation for possible escape (Pearson and Rowell 1977), crouching aphids might be less agile when responding to possible threats. Two minutes after a vibration to their host plant, when they were probably crouched according to our results, aphids almost did not respond to a breath cue, which is a reliable indication that a mammalian herbivore is about to eat their host plant (Ben-Ari and Inbar 2014). Reduced responsiveness to mammalian breath could make aphids crouching anticipatorily more susceptible to incidental ingestion. As winds are far more prevalent than mammalian herbivores in the Þeld, it is probably adaptive for aphids to take this risk. In conclusion, aphids behave in a way that reduces their chances of being removed from the plant by winds or a sudden blow to their host plant. By changing their body posture, aphids successfully attach themselves to the host plant and withstand the force exerted by wind bursts. This simple and effective behavioral solution probably exists in other plant-dwelling arthropods that are threatened by winds. As different cues that may indicate a windy environment may be interpreted in several ways, aphids Þne-tune their response and crouch either when wind is present or when a sudden wind burst is most likely to occur. Insect adhesion to plant parts to counter the danger of removal from the plant can thus be achieved not only by physiological and morphological mechanisms but also by behavior.
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Acknowledgments We thank two anonymous reviewers for their thorough examination of the article and very beneÞcial comments.
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Anticipatory and Reactive Crouching of Pea Aphids in Response to Environmental Perturbations MATAN BEN-ARI,1,2 STAV TALAL,3
AND
MOSHE INBAR1
Environ. Entomol. 43(5): 1319Ð1326 (2014); DOI: http://dx.doi.org/10.1603/EN14046
ABSTRACT Animals use different strategies to deal with changing environmental conditions. While standing and feeding on their host plant, aphids (Hemiptera: Aphididae) may be exposed to detrimental environmental perturbations, such as strong winds. If aphids are forcibly blown off the plant and spend time on the ground, they will face additional dangers by both ground-dwelling predators and detrimental soil temperature. It is therefore adaptive for aphids to behave in a way that lowers the risk of being removed from the plant. We observed that pea aphids (Acyrthosiphon pisum (Harris)) display a speciÞc crouched body posture, previously undescribed, which reduces their chance of being carried off from the plant by sudden winds. We exposed aphids in the laboratory to different cues indicative of a windy environment: wind, plant vibration, and visual stimuli. We found that aphids crouch in two situations: 1) reactively, when they are being pulled by a continuous gust of wind threatening to dislodge them. 2) Anticipatorily, when environmental cues, such as plant vibration or continuous movement near their host plant, may signify that sudden wind gusts are expected. Crouching aphids were less likely to be dislodged by a sudden air stream or plant vibration than were aphids that did not crouch. Crouching thus improves the aphidsÕ chances of remaining on their host plant under unfavorable environmental conditions. KEY WORDS Acyrthosiphon pisum, dropping response, environmental cue, incidental ingestion, wind
Many plant-dwelling insects spend most of their lives on various plant tissues, but they may be dislodged when natural enemies force them off the plant (Eisner and Aneshansley 2000) or when winds carry them off (Stork 1980). Once dislodged from the plant by winds, insects may be exposed to new, potentially detrimental abiotic conditions on the ground (e.g., AlonsoMejia and Arellano-Guillermo 1992) or ground-dwelling natural enemies (Losey and Denno 1998). To avoid these possible costs, insects and other invertebrates deal with winds in several ways. Some seek shelter in places that eliminate or reduce the effect of wind (Atkinson and Newbury 1984, Herberstein and Heiling 2001, Gish et al. 2011) and others hold on tightly to the substrate to avoid dislodgement (Duplouy and Hanski 2013). Insects have developed a variety of mechanisms to adhere to plant surfaces (Betz and Ko¨ lsch 2004) both at rest and when they are in danger of being dislodged. While there are many studies of the physiological (e.g., adhesive secretions) and morphological (e.g., special adhesive structures on tarsi) adaptations allowing insects to attach themselves to the surface (e.g., Eisner and Aneshansley 2000, Gorb and Gorb 1 Department of Evolutionary and Environmental Biology, University of Haifa, 199 Abba Hushi Av., Mt. Carmel, Haifa, 3498838, Israel. 2 Corresponding author, e-mail: [email protected]. 3 Department of Zoology, Tel-Aviv University, Ramat Aviv, TelAviv, 69978, Israel.
2002), few studies examined behavioral mechanisms that can reduce dislodgement. One such behavior is the altering of the insectÕs body posture to resist dislodgement. Surprisingly, even though the body posture of insects has been examined in a variety of contexts (e.g., Pearson and Rowell 1977, OÕNeill and Kemp 1992, Dejean 2011), few reports have associated this change in body posture with the attempt to withstand winds. In a rare example, Grace and Shipp (1988) found that grasshoppers assume a crouched body position and reduce their tendency to jump when wind speed increases. Aphids (Hemiptera: Aphididae) are small sap-sucking insects that might suffer dire consequences should they be forcibly removed from their host plant by winds. Aphids do not readily move from their feeding spot unless threatened or when feeding conditions on the plant deteriorate (Dill et al. 1990, Gish et al. 2010). Even when they do drop from their host plant, they reduce the chance of reaching the ground by holding on to lower leaves in the same plant (Ribak et al. 2013). The reason for this reluctance to drop is probably the various dangers that await aphids on the ground, including desiccation, ground-dwelling predators, and reduced feeding time (McAllister et al. 1990, Dill et al. 1990, Gish et al. 2012). While studying the escape behavior of pea aphids (Acyrthosiphon pisum (Harris)) (Ben-Ari and Inbar 2014), we noticed that some adult individuals that
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Fig. 1. An adult A. pisum on a fava bean leaf before (a) and during (b) a wind burst. During the wind stimulus the aphid is crouching, i.e., the abdominal side of the soma is pressed against the surface of the leaf and the antennae are lowered toward the aphidÕs back. (c) A schematic representation of the angles measured in the description of the crouching response: ␣, the angle between the body and the surface of the leaf; and , the angle between the antennae and the body. (d) The body-plant and body-antennae angles (means ⫾ SE) of crouching and noncrouching aphids. Asterisks denote statistically signiÞcant differences according to a StudentÕs t-test (P ⬍ 0.05, Ndisturbed ⫽ 12, Nundisturbed ⫽ 10).
were perched on plants that had been moved or experienced windy conditions displayed a unique, more crouched body posture. The abdominal side of these aphidsÕ soma was pressed against the surface of the leaf and the antennae were lowered toward the aphidÕs back (Fig. 1aÐ b). To the best of our knowledge, despite the extensive research done on aphid defense behaviors, such a crouching behavior and its adaptive value have never been mentioned in the literature. This crouching posture is not a general reaction to danger because aphids threatened by natural enemies or competitors display a variety of responses, including moving the antennae, recoiling, withdrawing the stylet, and even walking awayÑ but never crouching close to the plant (Dixon 1958; Dill et al. 1990; Stern
and Foster 1996; Hartbauer 2010; M.B.-A., unpublished data). In this study, we Þrst describe the crouching behavior and then address the following questions: A) What cues induce aphids to crouch? B) What is the adaptive value of this body posture? Does the crouched position reduce the chances of dislodgement from the plant? Materials and Methods Characterization of the Crouching Posture. Pea aphids were taken from a colony reared in the University of Haifa on Vicia faba L. broad bean plants in constant temperature of 20 Ð22⬚C, 50 Ð 60% relative humidity, and a photoperiod of 16:8 (L:D) h. In all ex-
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periments, we used only adult aphids, each used only once. To describe the crouching behavior, we placed aphids on the stem of a broad bean plant in a row (four aphids per plant), allowing us to photograph all aphids from the same plane, a left proÞle picture. We examined normally standing aphids after a 1 h rest (n ⫽ 10) and aphids that experienced environmental disturbance (n ⫽ 12). The plant of the disturbed group was lightly shaken by a single strike to the base of the plant using a plant-shaking device described by Ben-Ari and Inbar (2014). This device allows us to deliver a blow of repeatable strength with a carefully positioned rubber band. The photographs were enlarged on a computer screen to ease the measurements of the angle between the body axis and the plantÕs surface and the angle between the body axis and the third and fourth segments of the left antenna (see Fig. 1). The average angles of disturbed and undisturbed aphids were compared using a StudentÕs t-test. What Cues Cause Aphids to Crouch? We hypothesized that environmental stimuli that may dislodge aphids would induce the crouching response in aphids. In each of the following experiments, a colony of 10 Ð12 aphids was placed on a plant and allowed to settle for 2 h. Each type of stimulus was replicated 20 times. The treatments were arranged and mixed so that no complete set of replicates for a given treatment was performed in a single day. First, we tested whether aphids indeed crouched when exposed to wind that might dislodge them from the plant. We used a wind producing device (see details in Ben-Ari and Inbar 2014) to directly expose a group of 10 Ð12 aphids to a continuous airßow of 3.6 m/s from a 5 cm distance (the average wind speed measured in the spring over several days in an open Þeld in the Carmel Mt., when host plants are abundant and aphid colonies are at their peak). We noted the proportion of crouching aphids before the wind started, and then at 5, 30, 60, 120, 300, and 600 s. As even after 600 s (10 min) of continuous wind, most aphids were still crouched, we extended this examination. To test how long aphids would remain in this posture, we conducted a similar experiment in which we exposed the aphids to 60 min of continuous wind. It soon became clear that aphids crouch not only during wind bouts, but also minutes after the wind itself ceased. We tested whether aphids would also crouch when they encounter a short stimulus, one that could occur in a windy environment but does not persistently threaten to carry them off the plant. We used a short, 2-s wind gust from the wind producing device, and then examined the proportion of crouching aphids in the colony in the same times as in the continuous wind experiment. Plant vibration, which occurs because of the wind itself or because of blows from other moving plant parts, might also dislodge an aphid. We exposed the aphids to a vibration cue, using the aforementioned plant-shaking device that produces a single strike of repeatable magnitude to the base of the plant. We placed the device 2 cm above the base of the stem, waited 60 s to reduce any effect of the visual move-
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ment next to the plant (see Ben-Ari and Inbar 2014), and then applied the vibration. We examined the proportion of crouched aphids in the same aforementioned times. Both air movement and plant vibration are physical cues that might indeed dislodge an aphid. We tested whether detection of visual movement, which does not physically move the aphid but might be indicative of adverse conditions such as plant-parts moving in the wind or an approaching large predator, will also induce crouching in aphids. We exposed aphids to a visual stimulus without any air or plant movement. The visual cue consisted of a black rectangular object moving horizontally repeatedly from side to side on white background. This object was displayed on a 7.5 by 4.5 cm screen of a Samsung GT-S5620 mobile phone placed 5 cm from the aphid colony (as described in Ben-Ari and Inbar 2014). The screen was placed next to the aphid colony and the movie started after 60 s of a blank screen. The short visual cue consisted of the object moving from side to side for 2 s followed by a blank screen, and the continuous cue consisted of movement of the object throughout the treatment. Crouching proportions were noted in similar times as in the previous experiments. Because every aphid group was examined at each of the time intervals, the proportions of crouching aphids in a colony were statistically compared with a repeated-measures analysis of variance after arcsine of square-root transformation of proportion data with time interval as the repeated factor. When data were not normally distributed after transformation, they were compared using the corresponding nonparametric Friedman test. The Adaptive Significance of the Crouching Posture. To examine the possible adaptive value of crouching, we tested whether dropping from the plant while it is exposed to winds is more costly for aphids than dropping without winds because winds carry aphids away from the plant. When they drop to the ground, most aphids prefer to return to their host plant (Roitberg and Myers 1978, Gish and Inbar 2006) or catch on to lower leaves (Ribak et al. 2013). If winds carry the aphids away from the plant while they drop, it might be harder for them to locate a host. We placed 10 aphid colonies on 10-cm-tall fava bean plants (with the pot they were in, colonies were 20 cm off the surface of the table). We exposed the plants to winds of different velocities (0, 2.6, 3.6, and 4.6 m/s) and simultaneously induced the aphids to let go of their grip by using an apparatus emulating mammalian breath (as described in Gish et al. 2010, supplementary material), which causes many aphids to drop off their host plant. We examined the average horizontal distance of the dropping aphids from the base of the plant in each colony. This experiment was replicated eight times for each air-speed treatment (distances were averaged in each replication, so variability was reduced). As the variance of the data in the different groups was similar (according to LeveneÕs test), we performed a linear regression with wind velocity as the independent variable and distance of the landing
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Fig. 2. The proportion of crouching individuals (means ⫾ SE) from an aphid colony in response to a continuous gust of 3.6 m/s wind. In each bar N ⫽ 20 colonies of 10Ð12 aphids each. Control group was approached with the wind producing device but not subjected to wind. Every colony was examined at each of the times.
aphid from the base of the plant as the dependent variable. Crouching after an initial wind or vibration might also be adaptive if such a posture reduced the aphidsÕ chances of being dislodged by another sudden wind gust or plant vibration, for example, by improving their grip or reducing the windÕs drag on their bodies. To test this possibility, we examined whether aphids are able to reduce dislodgement by wind and plant vibration when they crouch. First, we tested whether noncrouching aphids might be dislodged by a powerful, sudden motion of air or of their host plant. We placed a single aphid on a fava bean plant and allowed it to rest for 2 h. We then exposed the aphids to one of two strong perturbations: 1) a stream of fast ßowing (8 m/s) air that was applied through a ßexible pipe held 5 cm from the aphid. 2) A strong vibration to the host plant, performed by pulling the rubber band in the plant vibration device to twice the usual distance. We examined the proportion of aphids that were dislodged by the wind or the strong vibration. We performed the same two treatments on aphids that were Þrst induced to crouch. Because preliminary results showed that the highest proportion of crouching was evident 60 Ð120 s after a vibration treatment, we induced crouching by applying an initial, regular vibration (that did not dislodge any aphid) and waiting 90 s before applying the strong vibration or wind gust. Every treatment was replicated 20 times, and the proportion of dislodged aphids was compared for each treatment (strong wind and strong vibration) between the crouching and noncrouching aphids using a Z-test for proportions. Results Characterization of the Crouching Response. After an environmental perturbation (gust of wind and plant vibration), aphids displayed a distinctive change in their body posture (Fig. 1aÐ b) in two main attri-
butes: They lowered their bodies and the angle between the body and the plant decreased threefold for crouching aphids (Fig. 1d, StudentÕs t-test; t ⫽ 4.498; df ⫽ 19; P ⬍ 0.001). The aphids also moved their antennae backwards and reduced the angle between the antennae and the body to nearly half of the angle in noncrouching aphids (StudentÕs t-test, t ⫽ 6.643; df ⫽ 18; P ⬍ 0.001). The Cues Inducing Aphids to Crouch. While before experiencing the cue aphids at rest hardly crouch (⬍10%), most of them crouched in response to a continuous wind gust pulling on their bodies and threatening to dislodge them. After 5 s of exposure to 3.6 m/s wind, most aphids (85Ð95%) were crouching and remained so even after 10 min of wind (Fig. 2). Only after an hour of continuous wind was there a decrease in the crouching proportion, with only 46.9 ⫾ 9.5% (mean ⫾ SD) of the aphids still crouching. Of the total aphids, 27.7 ⫾ 3% left the feeding place altogether to other locations on the plant or off the plant altogether. In the control group, which was not subjected to wind, only 3.3 ⫾ 1.4% of the aphids left the feeding place. The short cues elicited a different response (Fig. 3). After a 2-s wind gust or a vibration to the host plant, the aphids began to crouch, but not immediately. Only after 30 s did the proportion crouching gradually increase, reaching its peak 60 Ð120 s after the cue (79.9 ⫾ 3% in vibration cue and 70 ⫾ 3% in the wind cue). The proportion of crouching aphids then declined, returning to the initial levels 600 s after the cue. This change in crouching proportions was signiÞcant for both mechanical cues (wind: Friedman test, 2 ⫽ 109.373; df ⫽ 6; P ⬍ 0.001; vibration: Friedman test, 2 ⫽ 108.76; df ⫽ 6; P ⬍ 0.001). The aphids responded differently to the short and continuous visual cues (Fig. 4). While a short (2 s) visual cue did not induce crouching at all, as the visual disturbance continued, more and more aphids crouched, peaking at 60 s of continuous visual pertur-
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Fig. 3. The proportion of crouching individuals (means ⫾ SE) from an aphid colony in different time-lags after an initial short cue (2 s of 3.6 m/s wind or a single vibration to the base of the host plant). In each bar N ⫽ 20 colonies of 10Ð12 aphids each. The leftmost bar in both groups represents the proportion before the cue was applied.
bation (continuous visual: Friedman test, 2 ⫽ 109.105; df ⫽ 6; P ⬍ 0.001; short visual: Friedman test, 2 ⫽ 109.105; df ⫽ 6; P ⬍ 0.001). Afterwards, aphids slowly returned to a normal standing position. The Adaptive Value of Aphid Crouching. Strong winds caused dropping aphids to land further away from their host plant (Fig. 5), and thus most probably reduced their chances of returning to the same plant. Crouching aphids were far less likely to be dislodged (Fig. 6) by both a sudden gust of wind (Z-test for proportions, n1 ⫽ n2 ⫽ 20; Pcrouch ⫽ 0.25, Pnoncrouch ⫽ 0.85; Z ⫽ 3.814; P ⬍ 0.001) or by a strong vibration of their host plant (Z-test for proportions, n1 ⫽ n2 ⫽ 20; Pcrouch ⫽ 0.25, Pnoncrouch ⫽ 0.6; Z ⫽ 2.239; P ⫽ 0.025).
Discussion In this work, we described a new defense behavior of adult pea aphids: a crouching posture brought about by environmental cues. We found that by crouching pea aphids not only decrease the chance of being blown off a plant during a lengthy wind burst, but they also prepare for possible future bursts by changing their body posture in anticipation of possible future bursts. This anticipatory crouching posture allowed aphids to withstand sudden wind bursts and plant shaking and reduce the danger being dislodged by them. While we tested adult aphids, thirdÐfourth-instar nymphs perform this behavior as well (M.B.-A., unpublished data).
Fig. 4. The proportion of crouching individuals (means ⫾ SE) from an aphid colony in different times after a 2 s cue or during a long continuous visual cue. Each bar represents 20 colonies of 10Ð12 aphids each.
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Fig. 5. A linear regression of the distance of a dropping aphid from the basis of a 20 cm high plant as a dependent variable of the velocity of wind it was exposed to while dropping (P ⬍ 0.001).
Winds can affect aphids not only physically (by pulling on them and even dislodging them) but also physiologically. Winds can change the immediate physical environment of organisms and thus affect their water balance and thermoregulation (Kingslover and Watt 1983). Long exposure to wind may induce desiccation and cause stress and aphids dropped more readily in response to herbivore breath or even walked away from their feeding site after it was exposed to the prolonged wind bursts. Short wind bursts are less likely to desiccate an aphid but may affect its ability to remain on its host plant. Apterous aphids feed and stand on exposed plant parts and are therefore affected by sudden gusts of wind (Gish et al. 2011) and may be carried off the plant if they lose their grip. Many of the dropping aphids may return to their host plant (Calabrese and Sorensen 1978). Therefore, landing farther away from the host plant owing to winds could increase the time spent on the ground and substantially reduce the chances of an aphidÕs successful return. The main reason is that when traveling on the ground, aphids face the risk of predation, desiccation,
and loss of feeding time (Roitberg and Myers 1979, Gish et al. 2012). Hence, even when forced to drop, aphids attempt to grab plant parts on their way down to avoid reaching the ground (Ribak et al. 2013) and being carried away by wind, while dropping, will also reduce their chances of doing so. Crouching aphids are less likely to be dislodged by strong winds and plant vibration and can possibly reduce the chances of the unnecessary detrimental effects of time spent on the ground. Animals may behave in ways that do not necessarily match their current situation, but might be adaptive in the future (Correia et al. 2007). The behavioral mechanism that aphids use to counter dislodgement has at least two functions: reactive and anticipatory. Reactive responses are those that occur when a threat is present and evident and the response may lower the cost of this threat. Anticipatory behaviors are those that manifest without a threat present and reduce the possible costs should a threat appear suddenly (Cooper 1998). When aphids were exposed to a constant airßow, they reactively crouched and reduced the
Fig. 6. The proportion of aphids dislodged from the plant by a strong perturbation: sudden strong vibration or sudden strong wind burst. In each treatment N ⫽ 20. Crouching aphids are those that were subjected to a gentle vibration to the plant before the strong perturbation, inducing them to crouch.
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chances of being dislodged by the air pulling on their bodies, and indeed no aphid was blown off. The anticipatory reaction occurred when aphids detected a short cue indicating the chance of possible wind gusts in their environment, such as a short wind gust or plant vibration, and continued to crouch for some time. The anticipatory crouching did not start immediately after the short wind pulse or vibration cues, rather, its proportion increased during the Þrst 2 min after the cue. Cues such as plant vibration and air movement are somewhat unreliable, as they might arise not from winds but rather from a grazing mammalian herbivore approaching the aphidsÕ host plant (Ben-Ari and Inbar 2014). According to the latter study, in the Þrst few seconds after such cues, aphids are more inclined to drop from the plant, but after 30 s or more, as the unreliable cue is dissociated from mammalian presence and is interpreted as originating from winds, aphids are less likely to drop. The anticipatory crouching in this study shows the opposite trend from the tendency to drop from the plant reported in Ben-Ari and Inbar (2014). This contrast, higher crouching proportions coinciding with lower dropping tendencies, reinforces our interpretation that crouching aphids do so to lower the chances of being carried away by winds. Both modes of crouching (i.e., reactive and anticipatory) were very effective in dealing with the danger of dislodgement, but a sustained crouching posture may incur some cost. Though some insects crouch in preparation for possible escape (Pearson and Rowell 1977), crouching aphids might be less agile when responding to possible threats. Two minutes after a vibration to their host plant, when they were probably crouched according to our results, aphids almost did not respond to a breath cue, which is a reliable indication that a mammalian herbivore is about to eat their host plant (Ben-Ari and Inbar 2014). Reduced responsiveness to mammalian breath could make aphids crouching anticipatorily more susceptible to incidental ingestion. As winds are far more prevalent than mammalian herbivores in the Þeld, it is probably adaptive for aphids to take this risk. In conclusion, aphids behave in a way that reduces their chances of being removed from the plant by winds or a sudden blow to their host plant. By changing their body posture, aphids successfully attach themselves to the host plant and withstand the force exerted by wind bursts. This simple and effective behavioral solution probably exists in other plant-dwelling arthropods that are threatened by winds. As different cues that may indicate a windy environment may be interpreted in several ways, aphids Þne-tune their response and crouch either when wind is present or when a sudden wind burst is most likely to occur. Insect adhesion to plant parts to counter the danger of removal from the plant can thus be achieved not only by physiological and morphological mechanisms but also by behavior.
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Acknowledgments We thank two anonymous reviewers for their thorough examination of the article and very beneÞcial comments.
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