Spatiotemporal Analysis of Predation by Carabid Beetles (Carabidae) on Nematode Infected and Uninfected Slugs in the Field

Bjørn Arild Hatteland,William O C Symondson,Solveig Haukeland,Ian P Vaughan,Steffen Roth,May Bente Brurberg,Nicholas J Mills

doi:10.1371/journal.pone.0082142

Bjørn Arild Hatteland, William O C Symondson + Show 5 more

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https://doi.org/10.1371/journal.pone.0082142

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Abstract

The dynamics of predation on parasites within prey has received relatively little attention despite the profound effects this is likely to have on both prey and parasite numbers and hence on biological control programmes where parasites are employed. The nematode Phasmarhabditis hermaphrodita is a commercially available biological agent against slugs. Predation on these slugs may, at the same time, result in intraguild predation on slug-parasitic nematodes. This study describes, for the first time, predation by carabid beetles on slugs and their nematode parasites on both spatial and temporal scales, using PCR-based methods. The highest nematode infection levels were found in the slugs Deroceras reticulatum and Arion silvaticus. Numbers of infected slugs decreased over time and no infected slugs were found four months after nematode application. The density of the most abundant slug, the invasive Arion vulgaris, was positively related to the activity-density of the carabid beetle, Carabus nemoralis. Predation on slugs was density and size related, with highest predation levels also on A. vulgaris. Predation on A. vulgaris decreased significantly in summer when these slugs were larger than one gram. Predation by C. nemoralis on slugs was opportunistic, without any preferences for specific species. Intraguild predation on the nematodes was low, suggesting that carabid beetles such as C. nemoralis probably do not have a significant impact on the success of biological control using P. hermaphrodita.

Highlights

Trophic interactions are fundamental to ecology and spatial, as well as temporal, dynamics are essential to any understanding of such interactions [1]
The slugs A. silvaticus and A. distinctus were detected in the guts of beetles for up to 40h with median detection times of 27.9 h and 32.4 h, respectively (Figure 2)
The most abundant slugs in our field were D. reticulatum, A. silvaticus, A. distinctus and A. vulgaris, of which D. reticulatum was the most heavily infected by the nematodes

Summary

Introduction

Trophic interactions are fundamental to ecology and spatial, as well as temporal, dynamics are essential to any understanding of such interactions [1]. Slugs are a major part of the diet in these beetles [6,7,8], and Symondson et al [9] found a significant temporal effect of P. melanarius on slug population growth and a reverse effect on the nutritional status of beetles, and on their reproductive success. Most of these studies have focused only on the generalist P. melanarius which is an abundant species in arable fields. Arion vulgaris Moquin-Tandon 1855 ( regarded as non-topotype A. lusitanicus Mabille 1868) has spread to many parts of northern Europe during the last decades [15,16] and is one of the most damaging gastropod pests in gardens, pastures and field crops [17,18]

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