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Changes in behavior are unable to disrupt a trophic cascade involving a specialist herbivore and its food plant.

ABSTRACT: Changes in ecological conditions can induce changes in behavior and demography of wild organisms, which in turn may influence population dynamics. Black brant (Branta bernicla nigricans) nesting in colonies on the Yukon-Kuskokwim Delta (YKD) in western Alaska have declined substantially (~50%) since the turn of the century. Black brant are herbivores that rely heavily on Carex subspathacea (Hoppner's sedge) during growth and development. The availability of C. subspathacea affects gosling growth rates, which subsequently affect pre- and postfledging survival, as well as size and breeding probability as an adult. We predicted that long-term declines in C. subspathacea have affected gosling growth rates, despite the potential of behavior to buffer changes in food availability during brood rearing. We used Bayesian hierarchical mixed-effects models to examine long-term (1987-2015) shifts in brant behavior during brood rearing, forage availability, and gosling growth rates at the Tutakoke River colony. We showed that locomotion behaviors have increased (? = 0.05, 95% CRI: 0.032-0.068) while resting behaviors have decreased (? = -0.024, 95% CRI: -0.041 to -0.007), potentially in response to long-term shifts in forage availability and brood density. Concurrently, gosling growth rates have decreased substantially (? = -0.100, 95% CRI: -0.191 to -0.016) despite shifts in behavior, mirroring long-term declines in the abundance of C. subspathacea (? = -0.191, 95% CRI: -0.355 to -0.032). These results have important implications for individual fitness and population viability, where shifts in gosling behavior putatively fail to mitigate long-term declines in forage availability.

SUBMITTER: Lohman MG

PROVIDER: S-EPMC6509370 | biostudies-literature | 2019 May

REPOSITORIES: biostudies-literature

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Changes in behavior are unable to disrupt a trophic cascade involving a specialist herbivore and its food plant.

Lohman Madeleine G MG Riecke Thomas V TV Acevedo Cheyenne R CR Person Brian T BT Schmutz Joel A JA Uher-Koch Brian D BD Sedinger James S JS

Ecology and evolution 20190408 9

Changes in ecological conditions can induce changes in behavior and demography of wild organisms, which in turn may influence population dynamics. Black brant (Branta bernicla nigricans) nesting in colonies on the Yukon-Kuskokwim Delta (YKD) in western Alaska have declined substantially (~50%) since the turn of the century. Black brant are herbivores that rely heavily on Carex subspathacea (Hoppner's sedge) during growth and development. The availability of C. subspathacea a ...[more]

PMID: 31110679

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Project description:BackgroundPlants, plant-feeding insects, and insect parasitoids form some of the most complex and species-rich food webs. According to the classic escape-and-radiate (EAR) hypothesis, these hyperdiverse communities result from coevolutionary arms races consisting of successive cycles of enemy escape, radiation, and colonization by new enemy lineages. It has also been suggested that "enemy-free space" provided by novel host plants could promote host shifts by herbivores, and that parasitoids could similarly drive diversification of gall form in insects that induce galls on plants. Because these central coevolutionary hypotheses have never been tested in a phylogenetic framework, we combined phylogenetic information on willow-galling sawflies with data on their host plants, gall types, and enemy communities.ResultsWe found that evolutionary shifts in host plant use and habitat have led to dramatic prunings of parasitoid communities, and that changes in gall phenotype can provide "enemy-free morphospace" for millions of years even in the absence of host plant shifts. Some parasites have nevertheless managed to colonize recently-evolved gall types, and this has apparently led to adaptive speciation in several enemy groups. However, having fewer enemies does not in itself increase speciation probabilities in individual sawfly lineages, partly because the high diversity of the enemy community facilitates compensatory attack by remaining parasite taxa.ConclusionTaken together, our results indicate that niche-dependent parasitism is a major force promoting ecological divergence in herbivorous insects, and that prey divergence can cause speciation in parasite lineages. However, the results also show that the EAR hypothesis is too simplistic for species-rich food webs: instead, diversification seems to be spurred by a continuous stepwise process, in which ecological and phenotypic shifts in prey lineages are followed by a lagged evolutionary response by some of the associated enemies.

Project description:Host plant defenses are known to cascade up food chains to influence herbivores and their natural enemies, but how herbivore and predator traits and identity mediate such tri-trophic dynamics is largely unknown. We assessed the influence of plant defense on aphid and coccinellid performance in laboratory trials with low- vs. high-glucosinolate varieties of Brassica napus, a dietary specialist (Brevicoryne brassicae) and generalist (Myzus persicae) aphid, and five species of aphidophagous coccinellids. The performance of the specialist and generalist aphids was similar and unaffected by variation in plant defense. Aphid glucosinolate concentration and resistance to predators differed by aphid species and host plant defense, and these effects acted independently. With respect to aphid species, the dietary generalist aphid (vs. specialist) had 14% lower glucosinolate concentration and coccinellid predators ate three-fold more aphids. With respect to host plant variety, the high-glucosinolate plants (vs. low) increased aphid glucosinolate concentration by 21%, but had relatively weak effects on predation by coccinellids and these effects varied among coccinellid species. In turn, coccinellid performance was influenced by the interactive effects of plant defense and aphid species, as the cascading, indirect effect of plant defense was greater when feeding upon the specialist than generalist aphid. When feeding upon specialist aphids, low- (vs. high-) glucosinolate plants increased coccinellid mass gain by 78% and accelerated development by 14%. In contrast, when feeding upon generalist aphids, low- (vs. high-) glucosinolate plants increased coccinellid mass gain by only 11% and had no detectable effect on development time. These interactive effects of plant defense and aphid diet breadth on predator performance also varied among coccinellid species; the indirect negative effects of plant defenses on predator performance was consistent among the five predators when transmitted via the dietary specialist aphid, but these effects varied substantially among predators-in both the magnitude and direction-when transmitted via the dietary generalist aphid. Accordingly, the cascading effect of plant defense on predators was stronger in magnitude and more consistent among predator taxa when transmitted by the specialist than generalist herbivore. Overall, these findings support a central role of herbivore diet breadth in mediating both the strength and contingency of tri-trophic interactions.

Dataset Information

Changes in behavior are unable to disrupt a trophic cascade involving a specialist herbivore and its food plant.

Publications

Changes in behavior are unable to disrupt a trophic cascade involving a specialist herbivore and its food plant.

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