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Revisiting implementation of multiple natural enemies in pest management.

ABSTRACT: A major goal of biological control is the reduction and/or eradication of pests using various natural enemies, in particular, via deliberate infection of the target species by parasites. To enhance the biological control, a promising strategy seems to implement a multi-enemy assemblage rather than a single control agent. Although a large body of theoretical studies exists on co-infections in epidemiology and ecology, there is still a big gap in modelling outcomes of multi-enemy biological control. Here we theoretically investigate how the efficiency of biological control of a pest depends on the number of natural enemies used. We implement a combination of eco-epidemiological modelling and the Adaptive Dynamics game theory framework. We found that a progressive addition of parasite species increases the evolutionarily stable virulence of each parasite, and thus enhances the mortality of the target pest. However, using multiple enemies may have only a marginal effect on the success of biological control, or can even be counter-productive when the number of enemies is excessive. We found the possibility of evolutionary suicide, where one or several parasite species go extinct over the course of evolution. Finally, we demonstrate an interesting scenario of coexistence of multiple parasites at the edge of extinction.

SUBMITTER: Alharbi W

PROVIDER: S-EPMC9440112 | biostudies-literature | 2022 Sep

REPOSITORIES: biostudies-literature

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Revisiting implementation of multiple natural enemies in pest management.

Alharbi Weam W Sandhu Simran K SK Areshi Mounirah M Alotaibi Abeer A Alfaidi Mohammed M Al-Qadhi Ghada G Morozov Andrew Yu AY

Scientific reports 20220902 1

A major goal of biological control is the reduction and/or eradication of pests using various natural enemies, in particular, via deliberate infection of the target species by parasites. To enhance the biological control, a promising strategy seems to implement a multi-enemy assemblage rather than a single control agent. Although a large body of theoretical studies exists on co-infections in epidemiology and ecology, there is still a big gap in modelling outcomes of multi-enemy biological contro ...[more]

PMID: 36056142

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Project description:Invasive species pose a significant threat to biodiversity and agriculture world-wide. Natural enemies play an important part in controlling pest populations, yet we understand very little about the presence and prevalence of natural enemies during the early invasion stages. Microbial natural enemies of fall armyworm Spodoptera frugiperda are known in its native region, however, they have not yet been identified in Africa where fall armyworm has been an invasive crop pest since 2016. Larval samples were screened from Malawi, Rwanda, Kenya, Zambia, Sudan and Ghana for the presence of four different microbial natural enemies; two nucleopolyhedroviruses, Spodoptera frugiperda NPV (SfMNPV) and Spodoptera exempta NPV (SpexNPV); the fungal pathogen Metarhizium rileyi; and the bacterium Wolbachia. This study aimed to identify which microbial pathogens are present in invasive fall armyworm, and determine the geographical, meteorological and temporal variables that influence prevalence. Within 3 years of arrival, fall armyworm was exposed to all four microbial natural enemies. SfMNPV probably arrived with fall armyworm from the Americas, but this is the first putative evidence of host spillover from Spodoptera exempta (African armyworm) to fall armyworm for the endemic pathogen SpexNPV and for Wolbachia. It is also the first confirmed incidence of M. rileyi infecting fall armyworm in Africa. Natural enemies were localised, with variation being observed both nationally and temporally. The prevalence of SfMNPV (the most common natural enemy) was predominantly explained by variables associated with the weather; declining with increasing rainfall and increasing with temperature. However, virus prevalence also increased as the growing season progressed. The infection of an invasive species with a natural enemy from its native range and novel pathogens specific to its new range has important consequences for understanding the population ecology of invasive species and insect-pathogen interactions. Additionally, while it is widely known that temporal and geographic factors affect insect populations, this study reveals that these are important in understanding the distribution of microbial natural enemies associated with invasive pests during the early stages of invasion, and provide baseline data for future studies.

Project description:BACKGROUND:Biological invasions provide a window on the process of community assembly. In particular, tracking natural enemy recruitment to invading hosts can reveal the relative roles of co-evolution (including local adaptation) and ecological sorting. We use molecular data to examine colonisation of northern Europe by the parasitoid Megastigmus stigmatizans following invasions of its herbivorous oak gallwasp hosts from the Balkans. Local host adaptation predicts that invading gallwasp populations will have been tracked primarily by sympatric Balkan populations of M. stigmatizans (Host Pursuit Hypothesis). Alternatively, ecological sorting allows parasitoid recruitment from geographically distinct populations with no recent experience of the invading hosts (Host Shift Hypothesis). Finally, we test for long-term persistence of parasitoids introduced via human trade of their hosts' galls (Introduction Hypothesis). RESULTS:Polymorphism diagnostic of different southern refugial regions was present in both mitochondrial and nuclear microsatellite markers, allowing us to identify the origins of northern European invaded range M. stigmatizans populations. As with their hosts, some invaded range populations showed genetic variation diagnostic of Balkan sources, supporting the Host Pursuit Hypothesis. In contrast, other invading populations had an Iberian origin, unlike their hosts in northern Europe, supporting the Host Shift Hypothesis. Finally, both British and Italian M. stigmatizans populations show signatures compatible with the Introduction Hypothesis from eastern Mediterranean sources. CONCLUSIONS:These data reveal the continental scale of multi-trophic impacts of anthropogenic disturbance and highlight the fact that herbivores and their natural enemies may face very different constraints on range expansion. The ability of natural enemies to exploit ecologically-similar hosts with which they have had no historical association supports a major role for ecological sorting processes in the recent assembly of these communities. The multitude of origins of invading natural enemy populations in this study emphasises the diversity of mechanisms requiring consideration when predicting consequences of other biological invasions or biological control introductions.

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Revisiting implementation of multiple natural enemies in pest management.

Publications

Revisiting implementation of multiple natural enemies in pest management.

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