Dataset Information

Top-down and bottom-up controls on an herbivore on a native and introduced plant in a tropical agricultural landscape.

ABSTRACT: The recent introduction in a tropical agricultural environment of a weedy open-habitat plant (Solanum myriacanthum) and subsequent host range expansion of a common forest-edge butterfly (Mechanitis menapis) onto that plant provides an opportunity to examine reconfiguration of tritrophic networks in human-impacted landscapes. The objectives of this study were (1) determine if the caterpillars on the exotic host are more or less limited by plant defenses (bottom-up forces) and if they experience enemy release (decrease of top-down pressure) and (2) define how anthropic open pasture habitat influences the herbivore's tritrophic niche. Field and laboratory monitoring of larval survival and performance on a native (Solanum acerifolium) host plant and the exotic (S. myriacanthum) host plant were conducted in the Mindo Valley, Ecuador. Plant physical defenses were also measured. Results showed that larval mortality was mostly top-down on S. acerifolium, linked to parasitism, but mostly bottom-up on S. myriacanthum, possibly linked to observed increased plant defenses. Thus, in the absence of co-evolved relationships, herbivores on the exotic host experienced little top-down regulation, but stronger bottom-up pressures from plant defenses. These findings provide a rare empirical example of enemy-free space as a mechanism underlying host-range expansion. S. myriacanthum was less colonized in open pastures than in semi-shaded habitats (forest edges, thickets): fewer eggs were found, suggesting limited dispersal of adult butterflies into the harsh open environments, and the survival rate of first instar larvae was lower than on semi-shaded plants, likely linked to the stronger defenses of sun-grown leaves. These findings show how environmental conditions modulate the rewiring of trophic networks in heavily impacted landscapes, and limit a biocontrol by a native herbivore on an invasive plant in open habitats.

SUBMITTER: Despland E

PROVIDER: S-EPMC7075360 | biostudies-literature | 2020

REPOSITORIES: biostudies-literature

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Top-down and bottom-up controls on an herbivore on a native and introduced plant in a tropical agricultural landscape.

Despland Emma E Santacruz Paola G PG

PeerJ 20200313

The recent introduction in a tropical agricultural environment of a weedy open-habitat plant (<i>Solanum myriacanthum</i>) and subsequent host range expansion of a common forest-edge butterfly (<i>Mechanitis menapis</i>) onto that plant provides an opportunity to examine reconfiguration of tritrophic networks in human-impacted landscapes. The objectives of this study were (1) determine if the caterpillars on the exotic host are more or less limited by plant defenses (bottom-up forces) and if the ...[more]

PMID: 32206453

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Project description:Herbivore populations are regulated by bottom-up control through food availability and quality and by top-down control through natural enemies. Intensive agricultural monocultures provide abundant food to specialized herbivores and at the same time negatively impact natural enemies because monocultures are depauperate in carbohydrate food sources required by many natural enemies. As a consequence, herbivores are released from both types of control. Diversifying intensive cropping systems with flowering plants that provide nutritional resources to natural enemies may enhance top-down control and contribute to natural herbivore regulation. We analyzed how noncrop flowering plants planted as "companion plants" inside cabbage (Brassica oleracea) fields and as margins along the fields affect the plant-herbivore-parasitoid-predator food web. We combined molecular analyses quantifying parasitism of herbivore eggs and larvae with molecular predator gut content analysis and a comprehensive predator community assessment. Planting cornflowers (Centaurea cynanus), which have been shown to attract and selectively benefit Microplitis mediator, a larval parasitoid of the cabbage moth Mamestra brassicae, between the cabbage heads shifted the balance between trophic levels. Companion plants significantly increased parasitism of herbivores by larval parasitoids and predation on herbivore eggs. They furthermore significantly affected predator species richness. These effects were present despite the different treatments being close relative to the parasitoids' mobility. These findings demonstrate that habitat manipulation can restore top-down herbivore control in intensive crops if the right resources are added. This is important because increased natural control reduces the need for pesticide input in intensive agricultural settings, with cascading positive effects on general biodiversity and the environment. Companion plants thus increase biodiversity both directly, by introducing new habitats and resources for other species, and indirectly by reducing mortality of nontarget species due to pesticides. This study provides a comprehensive assessment of how habitat manipulation affects biocontrol services of a natural enemy community including both parasitoids and generalist predators. The trophic interactions between pests, parasitoids and predators were determined to achieve a better systemic understanding of top-down herbivore control, which can be strengthened when natural enemies complement each other or dampened by intraguild interactions. Our approach to selectively enhance the third trophic level to counteract specific herbivores was successful for both predators and parasitoids. Our results show significant positive effects of companion plants on predation of pest eggs and parasitism of pest larvae. Importantly, our data also suggest that carabids, staphylinids and spiders do not substantially interfere with parasitoid biocontrol as parasitoid DNA was rarely detected in predator guts.

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Dataset Information

Top-down and bottom-up controls on an herbivore on a native and introduced plant in a tropical agricultural landscape.

Publications

Top-down and bottom-up controls on an herbivore on a native and introduced plant in a tropical agricultural landscape.

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