Progress 09/01/06 to 08/31/11
Outputs
OUTPUTS: The non-consumptive effects of predators on herbivores account for approximately 50% of the reduction in plant damage predators provide. Therefore for effective biological control we must understand the factors in the agroecosystem that affect predation risk. This year we focused on the response of aphids to predation risk when on plants that vary in quality. The effects of predation risk and plant quality on aphid population growth and wing induction were tested in a fully randomized, factorial design field cage experiment. We varied plant quality using plants that vary in the expression of the jasmonate pathway, whereas predation risk was altered by comparing aphids in a predator-free environment with those experiencing either lethal or risk predators. Lethal predators were unaltered adult lady beetles; risk predators were lady beetles whose mandibles were glued to prevent them from consuming aphids. Overall project findings: The role of herbivory ontogeny (Thaler and Griffin 2008): This research is significant because it demonstrates that the non-consumptive effects of predators are substantial for caterpillars in several life stages. Interactions between host plant quality and predation risk (Kaplan and Thaler 2010): Because host plant quality is often manipulated in agricultural systems, it is important to understand how this alters the impact of biological control agents on pests. We found a large effect of plant quality on the predator-prey interaction. First, predators killed the most herbivores on the high quality plants and the fewest on the low quality plants. Second, plant quality modulated the non-consumptive effect of the predator on the prey. On the good quality plants, the non-consumptive effect of the predator was high. Metaanalysis of the interactions between host plant quality and omnivory (Kaplan and Thaler 2011): Omnivorous plant-feeding predators have been predicted to both increase and decrease prey consumption on resistant host-plants because of behavioral shifts in food preferences and direct ingestion of phytotoxins, respectively. To help resolve this debate, we reviewed the published literature on plant defense heteropteran interactions and found that the feeding ecology is highly contingent on plant defense expression. Prey responses to predation risk: How do animals balance growth and predator avoidance In a series of field and greenhouse experiments, we document that the tobacco hornworm caterpillar, Manduca sexta, reduces feeding by 30-40% due to risk of predation by stinkbugs, but develops more rapidly and gains the same mass as unthreatened caterpillars. Assimilation efficiency, extraction of nitrogen from food, and percent body lipid content all increased under predation risk, indicating that enhanced nutritional physiology allows caterpillars to compensate when threatened. Presentations: We presented our findings at the Ecological Society of America meeting in 2008, 2009, and 2010; Entomological Society of America meeting in 2011, International Plant Resistance Symposium in 2010, CSREES meeting in 2007, 2008 and 2010, and invited talks including Stockholm University and Texas A&M. PARTICIPANTS: Ian Kaplan (postdoctoral fellow) Monica Kersch-Becker (female graduate student) Scott McArt (graduate student) Suzi Claflin (female graduate student) Stuart Campbell (graduate student) Guilherme Becker (graduate student) Ordom Hout (minority undergraduate) Elena Olsen (female undergraduate) Isa Betancourt (female undergraduate) Jessica Nix (female technician) Alice Combs (female undergraduate) Liana Nice (female undergraduate) Stephanie Thornton (female undergraduate) Chris Roh (undergraduate) Ryan Reynolds (undergraduate) Andrew Mudge (undergraduate) Jerry Shen (undergraduate student) Linh Nguyen (undergraduate student) Marie Russell (female undergraduate student) Lukas Gonzalez (minority undergraduate) Adeolu Adeboye (undergraduate student) Marya Tsvetkova (female undergraduate student) TARGET AUDIENCES: Many minority and female undergraduate students were trained in the scientific method by working on this project. Many of these students are now pursueing graduate programs across the country. The results of this research were presented to the public at the Cornell Entomology Department's yearly open house. The research has been presented at numerous scientific meetings (see above)and in research papers for dissemination to the research community. PROJECT MODIFICATIONS: Not relevant to this project.
Impacts
Patterns of wing dimorphism were not different across plant treatments, which was somewhat unexpected given the dramatic differences in population growth. To our knowledge, wing response to phytohormonal manipulations has not been studied in any plant-aphid system. Despite the widely-held perception that low plant quality induces wing production, there have been mixed results across systems. Part of the complication is dissecting out the direct effect of plant quality vs. indirect effect of variation in crowding. Our finding that predation risk increased production of winged dispersal morphs adds to the existing literature on predator-induced life history changes in aphids. Patterns of wing dimorphism were not different across plant treatments, which was somewhat unexpected given the dramatic differences in population growth. Although predator-induced wing responses in our study were weakest on the highest quality plant (JA-deficient) and increased in magnitude thereafter, the statistical interaction between predator and plant-type treatments was non-significant. Thus, the combination of two stressors did not synergize wing production as we expected and has been shown in other studies. To our knowledge, wing response to phytohormonal manipulations has not been studied in any plant-aphid system.
Publications
- Kaplan, I and J.S. Thaler. 2011. Do plant defenses enhance or diminish prey suppression by omnivorous Heteroptera Biological Control, 59:53-60.
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Progress 09/01/09 to 08/31/10
Outputs
OUTPUTS: As we have demonstrated that both consumptive and non-consumptive effects of predators on prey are an important component of tritrophic interactions, we have been investigating the factors that influence their relative importance for several species of herbivorous insect species. In earlier years of this grant, we found that both the total effects of the predator and the consumptive and non-consumptive components are influenced by host plant quality. Previously, we had also done short term (2-3 day) experiments to show that the herbivores respond both behaviorally and physiologically to the presence of the predator. This year, we focused on understanding how the caterpillar integrates these physiological and behavioral responses over a longer portion of the larval period. In this set of experiments, we exposed 2nd instar caterpillars (Manduca sexta) to the presence of a predator (Podisus maculiventris) and measured the amount of leaf material eaten and weight gain every three days for 9 days. We exposed caterpillars to Risk predators that could hunt but not kill by removing the last millimeter of the predator beak so it cannot pierce the insect cuticle. Herbivores were caged using translucent spun polyester sleeves onto individual wild-type tomato plants with or without a Risk predator. Every three days, the caterpillars were weighed and moved to a new plant along with the predator if present. Leaf area eaten was measured on the plant the caterpillar had been feeding on after the caterpillar was moved to the next plant. By measuring consumption and growth, we were able to calculate conversion efficiencies as a measure of physiological digestive capacity. We also tested whether the caterpillar's physiological responses to the predator were simply an effect of reduced feeding or whether there was a specific response to the predator. We did this by manipulating food availability without the presence of a predator. Caterpillars were reared on tomato leaf disks in petri dishes for 36 hours. They were divided into three treatments receiving either 1) ad libitum food over the entire 36 hr period, 2) had ad libitum food for the first 28 hours and then no more food, 3) had the food removed for 3 3-hour periods over the course of the experiment which was then replaced. At the end of the 36 hour period all caterpillars were weighed and the total amount of food consumed measured. The first treatment shows how much they can grow with ad libitum food. The second treatment shows the effect of food limitation but with no warning of impending limitation. The third treatment shows the effect of food limitation when they are given a warning of food limitation and therefore the ability to adjust digestive efficiency in future feeding bouts. We presented our findings at the Ecological Society of America Annual meeting in August 2010 and will present a poster at the AFRI meeting in December 2010. PARTICIPANTS: Scott McArt, a graduate student in my lab received training by conducting the long-term experiment described above. Ian Kaplan, a postdoctoral researcher in my lab received training through the writing of the manuscript we published this year. Many undergraduates, including Ordom Huot a minority student, were involved with maintaining the insect colonies and rearing plants for experiments. TARGET AUDIENCES: Not relevant to this project. PROJECT MODIFICATIONS: Not relevant to this project.
Impacts
We found that the caterpillars adjust their behavioral and physiological responses over a 9-day predator exposure period. The caterpillars immediate response (within 45 minutes) is to reduce the time they spend moving on the plant. Over the first 3 days of predator exposure, they also reduce the amount of leaf consumption and compensate for this by increasing their digestive efficiency compared to predator-free control caterpillars. Between days 4-6 caterpillars in the predator treatment eat as much as the control caterpillars and their digestive efficiency also returns to levels lower or equal to the control caterpillars. Between days 7-9 the caterpillars in the predator treatment continue to eat as much as control caterpillars but manifest a cost of earlier feeding reductions with a decrease in digestive efficiency compared to controls. We also found that the response to the predator was not simply a result of the reduction in feeding. Caterpillars ate less and gained proportionately less weight in both treatments where they were starved, either with warning of impending food shortage or not. Since the caterpillars change their digestive efficiency in the presence of the predator, this is not simply due to the reductions in feeding in the presence of the predator. We have found that herbivores balance behavioral and physiological responses to predators over their larval period and that responses that appear "cost-free" in the short term can manifest themselves as costs later in life. This is important in considering the impact of a predator on its herbivore. Especially for herbivores where damage done later in life is most important for the plant (such as the case of M. sexta which does 90% of its feeding in the final instar), or pests with multiple generations per year, latent effects of early season predation could be important in understanding the total predator effect.
Publications
- Kaplan, I. and J.S. Thaler. 2010. Plant resistance attenuates the consumptive and non-consumptive impacts of predators on prey. Oikos 119:1105-1103.
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Progress 09/01/08 to 08/31/09
Outputs
OUTPUTS: As we have demonstrated that both consumptive and non-consumptive effects of predators on prey are an important component of tritrophic interactions, we have begun to investigate how herbivores behaviorally and physiologically respond to the presence of predators. Initially, we documented that Manduca sexta feed 50% less when in the presence of predators compared to when alone. We tested how both the behavioral and physiological responses of the herbivore to the predator are influenced by host plant quality. We manipulated resource quality by using three genetic lines of tomato plants to both increase and decrease plant quality: wild-type (with inducible resistance intact), jasmonate insensitive (non-inducible, highest quality) and jasmonate overexpressers (constitutively-induced, lowest quality). This summer, we focused on the interactions between the predator Podisus maculiventris and the prey is M. sexta. We manipulated the non-consumptive component by creating Risk predators. These are predators where the last millimeter of the beak is surgically snipped creating an individual who can hunt but not kill prey. Individual plants were caged, and a 3rd instar M. sexta was placed in the cage with or without an adult P. maculiventris. To determine how the M. Sexta physiology was affected by predator presence, we measured weight gain, leaf area consumption and frass production so that we could calculate nutritional indices. We also measured insect body composition. PARTICIPANTS: Nothing significant to report during this reporting period. TARGET AUDIENCES: Nothing significant to report during this reporting period. PROJECT MODIFICATIONS: Nothing significant to report during this reporting period.
Impacts
We found that even though the M. sexta eat 50% less in the presence of the predator these individuals gained the same amount of weight compared to caterpillars feeding in the absence of predators. Using nutritional indices, we demonstrated that this is because the consumptive efficiency is increased and they are able to extract more nutrients from the same amount of plant material when predators are present. What is additionally surprising is that the caterpillars could do this on both high and low quality plants. This suggests that over the short term (2 days) the caterpillars can compensate for reduced food intake. To search for a cost of this reduced feeding, we measured how lipid, carbohydrate and protein content of the caterpillar's are affected by the predator. We found that glycogen levels went down substantially in the presence of the predator. This could have long-term consequences for the performance of the caterpillars that would go undetected if consumption or weight gain were the only metrics of success utilized.
Publications
- J.S. Thaler and Griffin, C.A. 2008. Relative importance of consumptive and non-consumptive effects of predators on prey and plant damage: the influence of herbivore ontogeny. Entomologia Experimentalis et Applicata 128:34-40.
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Progress 09/01/07 to 08/31/08
Outputs
OUTPUTS: As we have demonstrated that both consumptive and non-consumptive effects of predators on prey are an important component of tritrophic interactions, we have begun to investigate the factors that influence their relative importance for several species of herbivorous insect species. Thus far, we have focused on the effects of host plant quality on predator-prey interactions. We tested how both the total effects of the predator and the consumptive and non-consumptive components are influenced by host plant quality. We manipulated resource quality by using three genetic lines of tomato plants to both increase and decrease plant quality: wild-type (with inducible resistance intact), jasmonate insensitive (non-inducible, highest quality) and jasmonate overexpressers (constitutively-induced, lowest quality). This summer, we focused on the interactions between the predator Podisus maculiventris and the prey is Trichoplusia ni. We manipulated the non-consumptive component by creating Risk predators. These are predators where the last millimeter of the beak is surgically snipped creating an individual who can hunt but not kill prey. Plants were caged in groups of two (of the same line) with 10 cm between each plant in translucent spun-polyester sleeves. These cages are closed on the top and buried into the soil on the bottom so they exclude most other organisms from entering. Each cage contains two plants so that the herbivores can potentially switch plants to avoid the predator and therefore predator pressure is not unnaturally high. Each cage of two plants was assigned to one of five treatments: control (no insects), herbivore only (six 3rd instar T. ni), lethal predator and herbivore (one adult P. maculiventris and six 3rd instar T. ni), risk predator and herbivore (one adult risk P. maculiventris and six 3rd instar T. ni). We presented our findings at two meetings this year, the Ecological Society of America Annual meeting in August 2008 and the CSREES meeting in November 2008. PARTICIPANTS: Ian Kaplan, postdoctoral associate TARGET AUDIENCES: Nothing significant to report during this reporting period. PROJECT MODIFICATIONS: Nothing significant to report during this reporting period.
Impacts
We have advanced our knowledge about how the non-consumptive effect of predators on prey alters feeding by several herbivores on host plants of differing quality. We found similar results to what we found with Manduca sexta that the non-consumptive effect of the predator is enhanced on high quality plants compared to low quality plants. We also found that T. ni respond differently to the predator than does M. sexta. T. ni drastically reduce the amount of moving they do within the plant but do not reduce the amount of feeding damage. Thus, patterns of feeding damage will be an important future metric potentially influencing plant performance. We have also found that the herbivore M. sexta alters its digestive physiology when in the presence of the predator. Even though the amount of leaf tissue consumed is reduced, the herbivore does not slow its growth due increased efficiency of digesting its food.
Publications
- No publications reported this period
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Progress 09/01/06 to 08/31/07
Outputs
OUTPUTS: As we have demonstrated that both consumptive and non-consumptive effects of predators on prey are an important component of tritrophic interactions, we have begun to investigate the factors that influence their relative importance. Thus far, we have focused on the effects of host plant quality on predator-prey interactions. We tested how both the total effects of the predator and the consumptive and non-consumptive components are influenced by host plant quality. We manipulated resource quality by using three genetic lines of tomato plants to both increase and decrease plant quality: wild-type (with inducible resistance intact), jasmonate insensitive (non-inducible, highest quality) and jasmonate overexpressers (constitutively-induced, lowest quality). The predator we use is Podisus maculiventris and the prey is Manduca sexta. We manipulated the non-consumptive component by creating Risk predators. These are predators where the last millimeter of the beak is surgically
snipped creating an individual who can hunt but not kill prey. Plants were caged in groups of two (of the same line) with 10 cm between each plant in translucent spun-polyester sleeves. These cages are closed on the top and buried into the soil on the bottom so they exclude most other organisms from entering. Each cage contains two plants so that the herbivores can potentially switch plants to avoid the predator and therefore predator pressure is not unnaturally high. Each cage of two plants was assigned to one of five treatments: control (no insects), herbivore only (six 3rd instar M. sexta), lethal predator and herbivore (one adult P. maculiventris and six 3rd instar M. sexta), risk predator and herbivore (one adult risk P. maculiventris and six 3rd instar M. sexta), and herbivore density control (six 3rd instar M. sexta). The herbivores in the Density treatment were compared to the Lethal treatment twice a day and caterpillars removed accordingly. We found a large effect of plant
quality on the predator-prey interaction. First, predators killed the most herbivores on the high quality plants and the fewest on the low quality plants. Second, plant quality modulated total effect as well as the non-consumptive effect of the predator on the prey. When we disentangle the mechanism of the effect of the predator on the prey, we find different paths on the high and medium quality plants. On the high quality plants, the non-consumptive effect of the predator was high. On these plants, exposure to the risk predator caused a great reduction in herbivore feeding damage but simply reducing herbivore density had no effect on subsequent feeding damage. On the medium quality plants, both consumptive and non-consumptive effects contributed. We have also conducted short term behavioral assays with the herbivore and predator to understand the patterns found in the field experiment. Results show that herbivores feed less in the presence of predators on high quality plants but not
low quality plants. Predators spend more of their time moving on the plant searching for prey on the high quality plants, this may explain the enhanced scaring component on these plants.
PARTICIPANTS: Jennifer Thaler (PI) Undergraduate assistants
Impacts
This research is significant because it demonstrates that the non-consumptive (scaring) effects of predators on prey are influenced by host plant quality. Because host plant quality is often manipulated in agricultural systems, it is important to understand how this alters the impact of biological control agents on pests.
Publications
- No publications reported this period
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